Abstract
The first reports that auxins promoted root formation in cuttings and that indole-3-butyric acid (IBA) was a particularly effective treatment date from the early 1930s. Since its introduction into horticultural practice, the focus on improvements in the rooting of plants has been largely on the proper use of auxins to enhance adventitious rooting (AR) as well as to increase the range of plants where it can be effective. In this review, we focus on new ideas that might build on what is known about auxin induction of AR. We explore what the evolution in chemical biology has opened through novel high-throughput screening tools to explore auxin regulation of plant development and what it might add to our understanding and potential to produce new tools for the manipulation of AR. The potential for using stronger auxin analogues, alternative indolealkanoic acids, compounds that alter β-oxidation of IBA and other indolealkanoic acids, auxin conjugates, inhibitors of auxin conjugation, inhibitors of endogenous auxin biosynthesis, as well as other plant hormones and compounds that inhibit the production or mimic the effects of signals that might be involved in AR are all discussed. The expectation is that a summary of these advances in our understanding of the chemical biology important to AR might increase the use and exploration of new ideas for the improvement in the practical approaches to advance horticultural rooting methods.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
The development of de novo roots, or new roots (Davies et al. 2018), on above-ground plant parts like stems is referred to as adventitious rooting (AR) or adventitious root formation (Roussos 2023). This process can occur naturally, sometimes serving as a survival response to abiotic stresses like flooding or salt exposure (Roussos 2023) or it can be induced artificially (Janick 1986) as a tool for producing new plants, including those grown in the horticulture industry. New plants regenerated or reproduced by nonsexual means, derived from plant tissues or plant parts, and not involving sexual recombination, have been propagated vegetatively (Janick 1986). With few exceptions, an explant generated using vegetative or clonal propagation techniques will maintain specific, desired characteristics and remain true-to-type (Dirr and Heuser 2006). The horticulture industry has thereby employed this phenomenon to overcome sexual reproduction barriers and commercialize the production of many desirable horticultural commodities and specialties ranging from ornamental crops to fruit, nuts, and vegetable crops (Davies et al. 1994). The ease of evoking AR on horticultural commodities can vary by species (Stokes et al. 2023) and for this reason, improving AR of desirable clones of plants has become a central theme of horticultural crop development and advancement (Davies et al. 2018), as well as profitability in the horticulture industry (Konjoian 2017). Advancing technologies or techniques that improve AR can yield increase in the diversity of plant selections cultivated, which subsequently become available for application by humans (Preece 2003). In a modern horticultural context, this trend can equate to economic opportunities for producers and broader crop and plant selection availability for consumers. There are a variety of factors that play a role in the success of AR formation on plants; however, this review explores the potential for using new opportunities for chemical biology to improve the AR of plants valuable for horticultural applications.
Early history
AR of fruit trees has a long history in the evolution of human behavior because under domestication the maintenance of desired genotypes becomes practical only by vegetative propagation (Zohary and Spiegel-Roy 1975; Weiss 2015). In fact, in very ancient writings, such as the Tanakh (Tanakh 1985), there are notations about “degenerate plants” that allude to the inherent problems of seed-propagated fruit crops. Propagation by cuttings was discussed in Book 2 of Historia Plantarum (Theophrastus; Einarson 1976) as well as in Natural History (Pliny the Elder; Anthony et al. 2010). The ability of people to select and maintain unique phenotypes likely advanced very early in human history and supported the change from a nomadic lifestyle to resident agriculture because fruit tree agriculture requires site-specific long-term residence. Fruit crops that can be easily propagated vegetatively could be considered preadapted for domestication (Zohary and Spiegel-Roy 1975; Zohary et al. 2012) and formed the basis for an early understanding of innate AR ability. However, it was a rich history that early agriculturists did not rely only on spontaneous rooting and treatments that accelerated root formation (Marston 1955). For example, Weaver (1972) discussed how, for centuries, farmers in Afghanistan and gardeners in Dutch used seeds of grains, such as barley, to induce rooting on cuttings. In addition, before the use of auxins specifically was established for rooting, treatments that likely resulted in a wound-auxin response (LaRue 1941; Xuan et al. 2008; Guo et al. 2008; Canher et al. 2020) were employed. These included manipulations such as simply cutting the stem itself or root removal (Steffens and Rasmussen 2016), as well as treatments with permanganate (Curtis 1918) or carbon monoxide (Zimmerman et al. 1933). In L.H. Bailey’s classic “The Nursery-Manual” (Bailey 1920), he notes three important conditions for successful “cuttage”: a moist and uniform atmosphere, porous soil, and sometimes bottom heat. Elevated root temperature was important in the 19th and early 20th century propagation greenhouse, and it could be due to an auxin regulatory mechanism, the increase in auxin levels with elevated temperature (Gray et al. 1998). Elevated temperature effects on auxin levels are mediated by phytochrome interacting factor 4 (PIF4; Franklin et al. 2011), thus it is connected to phytochrome regulated environmental treatments such as light quality and dark exposure periods (Halliday et al. 2009; Tillmann et al. 2022) that alter plant auxin responses. The early 20th century progress on AR was reviewed by Preece (2003).
Auxins and rooting
The first reports that auxins promoted root formation in cuttings were from Thimann and Went (1934), and Thimann and Koepfli (1935). Zimmerman and Wilcoxon (1935), and later Hitchcock and Zimmerman (1939) reported soon after about their studies on a variety of different auxin-like compounds, including indole-3-butyric acid (IBA) (see Table 1 for a list of compound abbreviations and acronyms). Zimmerman and Hitchcock trademarked IBA as Hormodin, and this started the first commercial use of IBA for rooting cuttings for propagation. In the subsequent decade, many compounds were tested in numerous trials for their ability to initiate AR, mainly with woody plant cuttings (Thimann and Behnke-Rogers 1950). Such early characterizations of auxins as “root-forming hormones” established a long-standing link between auxin and auxin-like compounds and root development (Went 1929; Thimann and Went 1934). Commercial plant propagation quickly recognized and adapted the technique of applying auxin for the rooting of stem cuttings of many forest and nursery crops. These techniques were applied to cuttings collected from taxa historically considered more challenging to root and greatly expanded the number of plants that could be propagated commercially. Evaluation of the merits of various auxin application methods continued through the second half of the 20th century (Huckenpahler 1955), with IBA as a basal quick-dip and powder application methods establishing themselves as the most broadly employed techniques in horticulture (Blythe et al. 2007; http://www.rooting-hormones.com/IBAmethd.htm; http://www.getroots.net/search.html; https://npn.rngr.net/npn/propagation).
When IBA was first found to have significant activity in the rooting process, it was widely assumed that it was a synthetic auxin, and in many growth bioassays, it was shown to be a weaker auxin than indole-3-acetic acid (IAA) (Woodward and Bartel 2005; Simon et al. 2013). A decade or more after its first uses for rooting were described, there appeared an early report of its presence in plants based on paper chromatography and bioassay in potato peelings (Blommaert 1954). It was also described as an endogenous auxin based on gas chromatography of extracts from Nicotiana (Bayer 1969). lBA was identified by gas chromatography-mass spectrometry (GC-MS) in pea root nodules (Badenoch-Jones et al. 1984) and reported in pea root and epicotyl (Schneider et al. 1985). Both free IBA and IBA released by hydrolysis from ester-conjugated lBA were clearly identified by GC-MS in the kernels and leaves of Zea mays (Epstein et al. 1989; Fallik et al. 1989; Ludwig-Müller and Epstein 1991) and subsequently in at least seven other plant species (Epstein and Ludwig-Müller 1993). Arabidopsis plants, for example, can accumulate a detectable amount of IBA (Epstein and Ludwig-Müller 1993). The endogenous presence of IBA is, however, somewhat inconsistent. For example, in maize, one variety exhibited detectable IBA and another did not (Epstein et al. 1989); in Arabidopsis, IBA has been found in both greater or lesser amounts, and in one study it was not detected at all (Novak et al. 2012). What controls the levels of endogenous IBA in specific varieties and growth conditions is not fully understood, although for Arabidopsis the pH of the growth medium, light intensity, and the volume of the culture flask can all have an effect (Ludwig-Müller et al. 1993). Similarly, the processes by which IBA is synthesized in plants need further clarification (Ludwig-Müller 2007; Damodaran and Strader 2019).
The biochemical conversion of IBA to IAA has been demonstrated in a variety of plants using isotope tracer methods (Epstein and Lavee 1984; Ludwig-Müller and Epstein 1991; Nordström et al. 1991; Van der Krieken et al. 1992; Baraldi et al. 1993, 1995; Kreiser et al. 2016). The isolation and characterization of mutants that are resistant to inhibitory concentrations of IBA or other long-side chain auxins but then respond normally to IAA or synthetic auxins has allowed the isolation of mutants defective in IBA responses, peroxisomal β-oxidation and peroxisome biogenesis (Zolman et al. 2000; Woodward and Bartel 2005; Baker et al. 2006; Damodaran and Strader 2019). The in vivo conversion of IBA to IAA involves six steps (Fig. 1), all essentially analogous to the β-oxidation of fatty acids: activation (thioesterification), oxidation, hydration, dehydration, thiolysis, and hydrolysis (Adham et al. 2005; Spiess and Zolman 2013; Rinaldi et al. 2016; Jawahir and Zolman 2021). IBA, or the synthetic auxin precursor 2,4-dichlorophenoxybutryric acid (2,4-DB) as well as chlorinated and dechlorinated IAAs, are converted to IAA or their respective analogues, indicating a somewhat permissive biochemical process. Following β-oxidation, the IAA- or auxin-like product that is generated seems to be exported from the peroxisomes. The genetic screens for Arabidopsis mutants resistant to exogenous IBA (initially named ibr, IBA resistant, or ped, peroxisome defective) has played an important role in our understanding of auxin metabolism and the special role IBA plays in this process. For example, the analysis of ech2 and other ibr mutants demonstrated that IBA-derived IAA plays an important role in root cell expansion (Strader et al. 2010b) as well as root hair and cotyledon cell expansion (Strader et al. 2010a, 2011). Although IBA application appears to have specificity for induction of root growth, it is nevertheless, only active upon its conversion to IAA (Strader et al. 2010b, 2011), indicating that it is an important auxin precursor rather than a weak auxin as originally proposed. This finding was confirmed when it was shown that the four-carbon side chain of IBA renders it unable to stimulate the formation of the TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALING F-BOX PROTEIN-Auxin/INDOLE-3-ACETIC ACID (TIR1/AFB-Aux/IAA) co-receptor complex required for auxin responsiveness (Uzunova et al. 2016). While studies have shown that IBA behaves differently than IAA and some have proposed it acts as a plant hormone itself (Van der Krieken et al. 1992, 1993; Chhun et al. 2004; Wang et al. 1994; Barnes 2011). Over the last two decades, the evolution of chemical biology has opened up novel high-throughput screening tools to explore auxin regulation of plant development (De Rybel et al. 2009), however, the use of these for the routine manipulation of plant materials has not replaced the regular use of IBA and other simple auxins. The goal of this review is to document the potential for both research and potential applications of the knowledge provided by these emerging discoveries. A summary of these chemical effectors and their target biochemical steps are shown in Fig. 3.
Hormonal pathways leading to root organogenesis required for adventitious root formation. Shown are the steps and pools of active compounds that are impacted by the synthetic compounds/agonists, inhibitors and activators discussed in the text. Compound abbreviations are consistent with what are defined in Table 1. IAA, indole-3-acetic acid; IBA, indole-3-butyric acid; NAA, 1-naphthaleneacetic acid; 4-CPA, 4-chlorophenoxyacetic acid; MCPA, 2-methyl-4-chlorophenoxyacetic acid; 2-DP, 2-(2,4-dichlorophenoxy) propionic acid; 4-Cl-IAA, 4-chloroindole-3-acetic acid; 5,6-diCl-IAA, 5,6-dichloroindole-3-acetic acid; 4-Cl-IBA, 4-chloroindole-3-butyric acid; 5,6-diCl-IBA, 5,6-dichloroindole-3-butyric acid; ICapA, indole-3-caproic acid; naxillin, (2E)-2-({5-[3-(trifluoromethyl) phenyl]-2-furyl} methylene) hydrazinecarbothioamide; 2,4DP-glyMe, 2-(2,4-dichlorophenoxy) propanoic acid-glycine methyl ester; 4-CPA-TrpMe, 4-chlorophenoxyacetic acid-L-tryptophan-O-methyl ester; JA, jasmonic acid; DHAP, 2,6-dihydroxyacetophenone; AIEP, adenosine-5’-[2-(1H-indol-3-yl) ethyl] phosphate; kakeimide, 4-(1,3-dioxoisoindolin-2-yl)-N-(3-isopropoxyphenyl) butanamide; nalacin, N-[4-[[6-(1H-pyrazol-1-yl)-3-pyridazinyl] amino] phenyl]-3-(trifluoromethyl)benzamide; IMT, indole-3-methyltetrazole; 4-Cl-IMT, 4-chloroindole-3-methyltetrazole; sortin2, 5-[[5-(3-chlorophenyl)-2-furanyl] methylene]-4-oxo-2-thioxo-3-thiazolidineethanesulfonic acid; retinal, (2E,4E,6E,8E)-3,7-dimethyl-9-(2,6,6-trimethylcyclohex-1-en-1-yl) nona-2,4,6,8-tetraenal; AVG, L-alpha-(2-aminoethoxyvinyl) glycine; AOA, 2-aminooxyacetic acid; rhizobitoxine, 2-amino-4-(2-amino-3-hydropropoxy)-trans-but-3-enoic acid; AIB, 2-aminoisobutyric acid; NBD, 2,5-norbornadiene; TCO, trans-cyclooctene, 1-MCP, 1-methylcyclopropene; triplin, 1-(1-morpholino-1-(thiophen-2-yl) propan-2-yl)-3-(2-(trifluoromethoxy) phenyl) thiourea; SHAM, salicylhydroxamic acid; DIECA, diethyldithiocarbamic acid; jarin-1, biphenyl-4-carboxylic acid [3-(3-methoxy-propionyl)-8-oxo-1,3,4,5,6,8-hexahydro-2H-1,5-methano-pyrido[1,2-a] [1,5] diazocin-9-yl]-amide; COMO, coronatine O-methyloxime; J4, 5-[3-(trifluoromethyl) benzylidene]-1,3-thiazolidine-2,4-dione; Y11, 2-ethoxy-4-(2-nitrovinyl) phenol; Y20, 4-hydroxy-3-[(4-methylcyclohexyl) carbonyl]-2H-chromen-2-one; lyn3, 3-[2-(Pyridin-4-yl) azepane-1-carbonyl]-1,2-dihydroisoquinolin-1-one; GA, gibberellins; H-acid, (1R,4R,5S,8S)-8-(hydroxymethyl)-1,7-dimethyl-4-propan-2-ylbicyclo [3.2.1] oct-6-ene-6-carboxylic acid; Compound 67D, (2(S)-3-phenyl-(9,10-dihydro-9,10-ethanoanthracene-11,12-dicarboximido) propanoic acid; Compound 6, (2(S)-3-methyl-(9,10-dihydro-9,10-ethanoanthracene-11,12-dicarboximido) penthanoic acid; AC94377, phthalimide 1-(3-chlorophthalimido)-cyclohexanecarboxamide; A1, N-(2-aminoethyl)-naphthalene-1-sulfonamide hydrochloride; TSPC, 3-(2-thienylsulfonyl) pyrazine-2-carbonitrile; SA, salicylic acid; chlormequat, 2-chloroethyl) trimethylammonium chloride; mepiquat, 1,1-dimethylpiperidinium chloride; chlorphonium, tributyl(2,4-dichlorobenzyl) phosphonium chloride; AMO-1618, N,N,N,2-tetramethyl-5-(1-methylethyl)-4-((1-piperidinylcarbonyl)oxy)benzenaminium chloride; ancymidol, cyclopropyl-(4-methoxyphenyl)-pyrimidin-5-ylmethanol; flurprimidol, 2-methyl-1-pyrimidin-5-yl-1-[4-(trifluoromethoxy) phenyl] propan-1-ol; HOE 074 784, 1-(2,6-diethylphenyl)-imidazole-5-carboxamide; tetcyclacis, 1-(4-chlorophenyl)-3a,4,4a,6a,7,7a-hexahydro-4,7-methano-1H-(1,2) diazeto (3,4f) benzotriazole; paclobutrazol, 1-(4-chlorophenyl)-4,4-dimethyl-2-(1,2,4-triazol-1-yl) pentan-3-ol; uniconazole, (S)-E-1-(4-chlorophenyl)-4,4-dimethyl-2-(1,2,4-triazole-1-yl) penten-3-ol; inabenfide, 4’-chloro-2’-(alpha-hydroxybenzyl)-isonicotinanilide; daminozide, 4-(2,2-dimethylhydrazinyl)-4-oxobutanoic acid; prohexadione, calcium 4-(1-oxidopropylidene)-3,5-dioxocyclohexanecarboxylate; trinexapac-ethyl, ethyl 4-[cyclopropyl(hydroxy)methylidene]-3,5-dioxocyclohexane-1-carboxylate; SL, strigolactones; TIS108, 6-phenoxy-1-phenyl-2-(1H-1,2,4-triazol-1-yl) hexan-1-one; abamine, methyl 2-[[(E)-3-(3,4-dimethoxyphenyl) prop-2-enyl]-[(4-fluorophenyl) methyl] amino] acetate; tebuconazole, 1-(4-chlorophenyl)-4,4-dimethyl-3-(1,2,4-triazol-1-ylmethyl) pentan-3-ol; 2-MN, 2-methoxy-1-naphthaldehyde; 4RG, 1-[4-(4-hydroxy-but-1-ynyl)-benzyl]-4-(3-trifluoromethyl-benzyl)-piperidine-4-carboxylic acid ethyl ester; TFQ0010, (3R, 4S)-3-methyl-4-phenethyloxetan-2-one; rhodestrin, (2E,4E,6E,8E,10E,12E,14E,16E,18E)24-hydroxy-2,6,10,14,19 pentamethyltetrecosa-2,4,6,8,10,12,14,16,18nonenyl-2(hydroxymethyl)-1H-indole-3-carboxylate
Stronger auxins for rooting
Auxins used to induce rooting are active in high concentration dips, often at 2000 mg/L (10 mM IBA) or higher, so it may be a reasoned consideration to employ “strong” auxins to lower the required concentrations or induce rooting in recalcitrant genotypes. Auxin-like compounds considered “strong” auxins include the auxinic herbicides, which typically cannot be applied at concentrations near the high-inductive doses often required due to phytotoxicity (Bottoms et al. 2011). Some have observed that auxinic herbicides at lower concentrations often induce callus and not AR (Verstraeten et al. 2013), although induction of AR has been noted as an aspect of herbicide damage (Warmund et al. 2021). The discovery of the TIR1/AFB-Aux/IAA auxin receptor (see Morffy and Strader 2022) has, nevertheless, renewed interest in auxins with very high receptor binding and less herbicidal effects. These include synthetic auxins such as NAA, 2,4-D, 4-chlorophenoxyacetic acid (4-CPA), 2-methyl-4-chlorophenoxyacetic acid (MCPA), and 2-(2,4-dichlorophenoxy) propionic acid (2-DP). In addition, 4-chloroindole-3-acetic acid (4-Cl-IAA), a naturally occurring auxin (Magnus et al. 1997), as well as related Cl-IAAs (Antolic et al. 1999) including 5,6-dichloroindole-3-acetic acid (5,6-diCl-IAA), have very high auxin activity, ranging from 10X that of IAA to 20X or more in some growth assays. Tests with many chloro-substituted IAAs found these forms to be quite active auxins (Engvild 1994; Antolic et al. 1999) rather than toxic (Slovin 1997) and this phenomenon has been confirmed in several studies. In fact, many of the monochloro and di-chloro-IAA compounds were later shown to have very high TIR1/AFB-Aux/IAA receptor binding activity (Jayasinghege et al. 2019) and minimal toxicity. Few root-induction or growth studies have further tested these compounds in practice. When tested, halogenated auxins showed promise for root induction. 5,6-diCl-IAA-methyl ester treatment significantly increased root numbers on hypocotyl cuttings of mung bean at a lower concentration than IBA (Pan and Tian 1999). Most reports were tests in bioassays other than difficult-to-root systems, possibly because they are considered rare compounds. Fortunately, facile methods for their synthesis exist (Cohen et al. 2022) and some are currently commercially available. IBA derivatives like 4-Cl-IBA and 5,6-diCl-IBA have received scant attention, although an old patent was issued (Marumo et al. 1991). We have found in preliminary studies that the halogenated IBAs have significant activity in vitro, suggesting that they are processed in the peroxisome like IBA to yield the active halogenated auxin.
Other unusual substituted IAAs have also been tested for enhanced rooting ability. For example, 4-trifluoromethylindole-3-acetic acid (4-TFM-IAA) was shown to be about 50% better than IBA at root induction in black gram [Vigna mungo (L.) Hepper] cutting, but only half as effective as 4-Cl-IAA (Katayama et al. 2008). α-Alkyl IAA derivatives were described as small-molecule agonists and antagonists of TIR1 receptor function (Hayashi et al. 2008), making them excellent candidate molecules for studies of AR, but at least in the initial reports, this biological activity was not studied.
Longer sidechain indolealkanoic acids
IAA almost never works as well as IBA at inducing rooting, and this observation has perplexed plant propagators who have not yielded a satisfactory explanation of why this happens. In some biological assays of root formation, IAA and IBA act quite differently (Chhun et al. 2004). IBA is predominantly moved as conjugates (Liu et al. 2012) but also has unique uptake mechanisms and is a saturable process (Rashotte et al. 2003), suggesting IBA uptake is carrier mediated and distinct from those involved in IAA uptake (Michniewicz et al. 2014; Frick and Strader 2018). The observation that plants convert IBA to IAA seemed to provide an easy answer to why IBA was effective (Kreiser et al. 2016). However, when concentrations of applied IAA and IBA were used on apple cuttings to produce a similar increase in internal IAA levels, IBA still gave more roots than IAA (Van der Krieken et al. 1992, 1993), so this simple idea cannot be the whole story. Although longer-side chain indolealkanoic acids have shown biological activity in growth studies comparable to that of IAA or IBA (Fawcett et al. 1960), their use in root induction appears to not have been done in difficult-to-root plants, and there is not much information on their utility (Van der Krieken et al. 1997). As with IBA, the metabolic fate of indole-3-caproic acid (ICapA; C6) is not certain, although it would be expected to mimic IBA in some regards but requires two rounds of β-oxidation to reduce the side chain from six carbons to two (Song et al. 2021). Understanding longer-chain compounds could help understand the differences between IAA and IBA in terms of the developmental signaling leading to AR initials. Also, as one increases the chain length, the compounds become more lipophilic, which could change uptake properties and require more β-oxidation activity to derive IAA. Compounds synthesized with up to an 11-carbon side chain, indole-3-undecanoic and (IUndecA; C11), have been reported. The longest even-numbered side chain for which a published synthesis is available appears to be indole-3-octanoic acid (IOctA; C8) (Avramenko et al. 1970), although the decanoic acid compound (C10) should be possible by the same procedures.
Increase rates of β-oxidation
The conversion of IBA → IAA and perhaps ICapA → IBA → IAA and longer chain conversions can also be studied in the presence of the non-auxin probe naxillin that appears to increase IBA → IAA conversion by β-oxidation in the root cap (De Rybel et al. 2012). Mutant analyses suggest that naxillin requires the endogenous IBA conversion pathway and thus acts through IBA-derived IAA to promote the development of lateral roots. Its function in tissues other than the root cap has not been extensively investigated, nor has its effect in AR or on auxin metabolism beyond the targeted reaction IBA → IAA been reported. However, other than attempting to increase the rate of uptake of IBA by methylation (Avery et al. 1937; Zimmerman and Hitchcock 1939; Rayle et al. 1970; Schenck et al. 2010) and optimization of methods of application (Blythe et al. 2007), there are few alternative chemical approaches for altering the efficacy of IBA itself.
A so-far unexplored method for up-regulating the targeted reaction IBA → IAA might be to change the carbon source for explants to favor enhanced peroxisome function. Peroxisome biology is complex, but it is clear that both stress and the need for fatty acid β-oxidation results in significant changes in metabolic capacity (Pan et al. 2020) and rates of pexophagy (Reumann and Bartel 2016). Application of mild stress or growth on fatty acids enriched media could potentially change the capacity of plants in tissue culture for higher peroxisome functions (Poirier et al. 1999) and thus potentially improve IBA → IAA activity.
Auxin conjugated forms
Auxin conjugation appears to play an important and complex role in the efficacy of AR (Haissig 1974). Landmark studies by Haissig (1989) described several esters of IAA and IBA for use in cutting propagation (Boyles et al. 1983). These included the aryl ester and aryl amide forms of IAA and IBA referred to as phenyl-IAA, phenyl-IBA, phenyl thioester-IBA, and phenyl amide-IBA. Their study showed these compounds to be more effective alternatives to the use of IAA, IBA, and NAA. Such modified derivatives have not received wide attention but have been reported to improve rooting and growth in oak and maple (Struve and Arnold 1986a, b; Struve and Rhodus 1988). While the role of conjugation remains complicated with many unresolved issues regarding its role in AR regulation, progress with the development of methods to study this has been observed in recent years. In Arabidopsis, the argonaute1 (ago1) mutants rarely form AR, and AUXIN RESPONSE FACTOR 17 (ARF17), which represses Gretchen Hagen 3 (GH3) gene expression and, thus, auxin conjugation, negatively regulates AR formation in ago1 mutants (Pacurar et al. 2014). Earlier studies of the metabolic fate of applied IBA showed that indole-3-butyryl-L-aspartate (IBAsp) levels reached a maximum 1 day after IBA treatment of cuttings. The conjugates thus formed were active in inducing the rooting of cuttings, with IBAsp being superior to free IBA. It was suggested that IBAsp might serve as an important source of auxin during later steps in AR (Wiesman et al. 1989; Riov 1993). Other IBA conjugates, such as IBAla, have also shown higher activity than IBA (Epstein and Wiesman 1987; Mihaljević and Salopek-Sondi 2012), while under specific conditions, IAA conjugates have also shown activity (Zelená and Fuksová 1991). Several different “slow release” forms have been tested for rooting, including different linkages to bovine serum albumin as well as IBA-anhydride, IBA-amino acids, IBA-polyamine-IBA, and IAA-polyamine-IAA, some with significantly positive results (Van der Krieken et al. 1997). Some synthetic auxin conjugates have shown rooting activity even when their “parent compound” was less effective. For example, auxin conjugate 2-(2,4-dichlorophenoxy) propanoic acid-glycine methyl ester (2,4DP-glyMe) was effective for vegetative propagation of mature pine tree cuttings (Riov et al. 2020). A recent report using a focused chemical screen of conjugated forms of four synthetic auxins (NAA, 2-DP, MCPA, and 4-CPA) identified 4-chlorophenoxyacetic acid-L-tryptophan-O-methyl ester (4-CPA-TrpMe) as enhancing the effect of K-IBA on AR in several recalcitrant woody plants (Roth et al. 2024). 4-CPA-TrpMe was shown not to interact directly with the TIR1-Aux/IAA7 auxin-perception complex, thus the activity seems to be related to the slow release of 4-CPA. However, it should be noted that tryptophan conjugates of IAA or jasmonic acid (JA) are endogenous auxin inhibitors (Staswick 2009). Indole-3-acetyl-L-tryptophan (IATrp) inhibited root gravitropic growth in seedlings, greatly reduced root inhibition from applied IAA, and inhibited the stimulation of lateral roots by IAA (Staswick 2009). Finally, and possibly related, various conjugates of 3-phenyllactic acid and tryptophan and esters of the conjugates showed good rooting activity in an Adzuki bean bioassay (Maki et al. 2022). While in combination, these studies would suggest that the ability to form and hydrolyze conjugates is important for AR, the issue is far from resolved (Salope-Sondi et al. 2015).
Inhibiting the induction of amide conjugation
While studies with applied auxin conjugates, mutants in conjugation, and the process of conjugation during IBA application logically all seem to suggest that conjugate formation and hydrolysis are both important aspects of AR, the results with small molecule inhibitors of auxin conjugation point to a specific role for conjugate formation. The first reported inhibitor of auxin amino acid conjugation, 2,6-dihydroxyacetophenone (DHAP) (Lee and Starratt 1986), doubled the number of roots in IBA treated cuttings (Epstein et al. 1993). Better characterized inhibitors of IAA-amido synthetase activity such as adenosine-5’-[2-(1H-indol-3-yl) ethyl] phosphate (AIEP), which mimics the adenylated intermediate of the GH3 auxin-amido synthetase reaction (Böttcher et al. 2012), bring specificity to studies of the enzyme activity resulting in indole auxin amino acid conjugation. Cano et al. (2018) found that in difficult-to-root carnation stem cuttings enhanced conjugation of auxin by GH3 enzymes leads to poor AR, and rooting ability could be restored with AIEP, the inhibitor of conjugation. After the description of AIEP, kakeimide (Hayashi et al. 2021; Fukui et al. 2022) and nalacin (** functions in their signal pathways that regulate aspects of plant development including root growth and tissue expansion. Both auxin and GA signaling have several points of convergence that allow crosstalk for the regulation of developmental events (Franklin et al. 2011; Richter et al. 2013), but they are not redundant in their functions. However, GA could apparently alleviate aspects of Aux/IAA gain-of-function phenotypic expression (Frigerio et al. 2006). Such studies suggest that changes in GA levels can, in part, also mediate aspects of auxin developmental activities (Hanson 1976). Other studies suggest that GA inhibits the formation of AR in plants by disrupting endogenous hormonal processes, including hormone levels and auxin transport (Willige et al. 2011; Mauriat et al. 2014; Li et al. 2023); however, the precise regulatory basis for “the observed interactions in root formation and plasticity are still to be discovered”.
Conclusions and perspectives
The discovery of the effects of IBA on AR 90 years ago had a profound impact on applied plant propagation methodology, bringing new forests, gardens, and fruit crops into wider use. AR, however, is a complex response, as might be expected for the generation of new organs from differentiated or partially differentiated tissues. The AR response is also sensitive to the plant’s environment, including light or darkness (Monteuuis and Bon 2000; Sorin et al. 2005; Klopotek et al. 2010; Pincelli-Souza et al. 2022), temperature (Corrêa and Fett-Neto 2004), as well as stress factors such as water availability and mineral nutrition (De Almeida et al. 2017). Regardless of the advances in research that have established IBA natural occurrence, the conversion of IBA to IAA as a critical process, and an array of hormonal and environmental needs, most of the commercial plant propagation remains primarily focused on the proper application of IBA, NAA, or combinations of the two (Sharma and Thapa 2022). It should be possible to do better, and as outlined in the review there are several opportunities to improve and many avenues to explore. A quickly evolving library of chemical effectors suggests new opportunities for future investigations that will allow us not only practical avenues for pretreatments but will also enable us to identify the molecular and signal transduction mechanisms underlying adventitious rooting as a key determinant in clonal propagation efficiency. A better understanding of cellular signals and regulatory cascades in development that are involved in adventitious root formation, underpinned by advances in systems and chemical biology, will provide a more complete understanding of rooting recalcitrance. It is the hope of this review that it will encourage a 21st century effort to bring new ideas to both research and the application of AR for plant improvement.
Availability of data and materials
There are no original datasets that were either generated and/or analyzed during the preparation of this review article.
References
Adham AR, Zolman BK, Millius A, Bartel B. Mutations in Arabidopsis acyl-CoA oxidase genes reveal distinct and overlap** roles in β-oxidation. Plant J. 2005;41:859–74. https://doi.org/10.1111/j.1365-313X.2005.02343.x.
Alallaq SAJ. Characterization of adventitious root formation in Populus species and Norway spruce. 2021. http://www.diva-portal.org/smash/get/diva2:1548864/FULLTEXT01.pdf. Accessed 1 Dec 2023.
Altamura MM, Piacentini D, Della Rovere F, Fattorini L, Falasca G, Betti C. New paradigms in brassinosteroids, strigolactones, sphingolipids, and nitric oxide interaction in the control of lateral and adventitious root formation. Plants. 2023;12:413. https://doi.org/10.3390/plants12020413.
Anthony G, Most GW, Settis S. The classical tradition. Cambridge, Massachusetts, and London: Harvard University Press; 2010.
Antolic S, Salopek B, Kojic-Prodic B, Magnus V, Cohen JD. Structural characterization and auxin properties of dichlorinated indole-3-acetic acids. Plant Growth Regul. 1999;27:21–31. https://doi.org/10.1023/A:1006031527789.
Arya A, Husen A. Chapter 9 - role of various auxins in adventitious root formation. In: Husen A, editor. Environmental, physiological and chemical controls of adventitious rooting in cuttings, a volume in plant biology, sustainability and climate change. London,: Academic; 2022. p. 213–38.
Atkinson JA, Rasmussen A, Traini R, Voß U, Sturrock C, Mooney SJ, et al. Branching out in roots: uncovering form, function, and regulation. Plant Physiol. 2014;166:538–50. https://doi.org/10.1104/pp.114.245423.
Avery GS, Burkholder PR, Creighton HB. Avena coleoptile curvature in relation to different concentrations of certain synthetic substances. Amer J Bot. 1937;24:226–32. https://doi.org/10.1002/j.1537-2197.1937.tb09094.x.
Avramenko VG, Pershin GN, Mushulov PI, Makeeva OO, Eryshev BY, Shagalov LB, et al. Indole derivatives. V. Synthesis and tuber culostatic activity of ω-(3-indolyl)-alkanoic acids. Pharm Chem J. 1970;4:135–7. https://doi.org/10.1007/BF00760970.
Badenoch-Jones J, Summons RE, Rolfe BG, Letham DS. Phytohormones, Rhizobium mutants and nodulation in legumes 1: III. Auxin metabolites in pea rot nodules. J Plant Growth Regul. 1984;3:23–9. https://doi.org/10.1104/pp.73.2.347.
Bai T, Dong Z, Zheng X, Song S, Jiao J, Wang M, et al. Auxin and its interaction with ethylene control adventitious root formation and development in apple rootstock. Front Plant Sci. 2020;11:574881. https://doi.org/10.3389/fpls.2020.574881.
Bailey LH. The nursery-manual: a complete guide to the multiplication of plants. New York: Macmillan; 1920.
Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL. Chewing the fat: β-oxidation in signalling and development. Trends Plant Sci. 2006;11:124–32. https://doi.org/10.1016/j.tplants.2006.01.005.
Baraldi R, Bertazza G, Predieri S, Cohen JD. Uptake and metabolism of indole-3-butyric acid during the in vitro rooting phase in pear cultivars (Pyrus communis). Acta Hort. 1993;329:289–91. https://doi.org/10.17660/ActaHortic.1993.329.68.
Baraldi R, Bertazza G, Bregol A, Fasolo F, Rotondi A, Predieri S, et al. Changes in auxins and polyamines during in vitro root induction on microcuttings of pear with different rooting response to indolebutyric acid. Plant Growth Regul. 1995;14:49–59. https://doi.org/10.1007/BF00212646.
Barnes HW. Plant hormones: the auxins, points for understanding their actions and use. Comb Proc Int Plant Propagators’ Soc. 2011;61:320–8.
Bayer MH. Gas chromatographic analysis of acidic indole auxins in Nicotiana. Plant Physiol. 1969;44:267–71. https://doi.org/10.1104/pp.44.2.267.
Bellini C, Pacurar DI, Perrone I. Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol. 2014;65:639–66. https://doi.org/10.1146/annurev-arplant-050213-035645.
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003;115:591–602. https://doi.org/10.1016/s0092-8674(03)00924-3.
Berthon JY, Ben Tahar S, Gaspar TH, Boyer N. Rooting phases of shoots of Sequoiadendron giganteum in vitro and their requirements. Plant Physiol Biochem. 1990;28:631–8.
Binder BM. Ethylene signaling in plants. J Biol Chem. 2020;295:7710–25. https://doi.org/10.1074/jbc.REV120.010854.
Blakesley D. Auxin metabolism and adventitious root initiation. In: Davis TD, Haissig BE, editors. Biology of adventitious root formation. Boston: Springer; 1994. p. 143–54.
Blakesley D, Weston GD, Elliott MC. Endogenous levels of indole-3-acetic acid and abscisic acid during the rooting of Cotinus eoggygria cuttings taken at different times of the year. Plant Growth Regul. 1991;10:1–12. https://doi.org/10.1007/BF00035126.
Blommaert KLJ. Growth- and inhibiting-substances in relation to the rest period of the potato tuber. Nature. 1954;174:970–2. https://doi.org/10.1038/174970b0.
Blythe EK, Sibley JL, Tilt KM, Ruter JM. Methods of auxin application in cutting propagation: a review of 70 years of scientific discovery and commercial practice. J Environ Hort. 2007;25:166–85. https://doi.org/10.24266/0738-2898-25.3.166.
Böttcher C, Dennis EG, Booker GW, Polyak SW, Boss PK, Davies C. A novel tool for studying auxin-metabolism: the inhibition of grapevine indole-3-acetic acid-amido synthetases by a reaction intermediate analogue. PLoS One. 2012;7:e37632. https://doi.org/10.1371/journal.pone.0037632.
Bottoms SL, Webster EP, Hensley JB, Blouin DC. Effects of herbicides on growth and vegetative reproduction of cree** rivergrass. Weed Tech. 2011;25:262–7. https://doi.org/10.1614/WT-D-10-00113.1.
Boyles DA, Gaines JR, Haissig BE. Auxin compositions of phenyl thioesters of indole-3-alkanoic acids and their use as auxin growth regulators. 1983. https://www.freepatentsonline.com/4415350.html. Accessed 1 Dec 2023.
Briggs D. Gibberellin-like activity of helminthosporol and helminthosporic acid. Nature. 1966;210:418–9. https://doi.org/10.1038/210418b0.
Brumos J, Robles LM, Yun J, Vu TC, Jackson S, Alonso JM, et al. Local auxin biosynthesis is a key regulator of plant development. Dev Cell. 2018;47:306–18.e5. https://doi.org/10.1016/j.devcel.2018.09.022.
Butler LG. Chemical communication between the parasitic weed Striga and its crop host. A new dimension in allelochemistry. In: Inderjit KM, Dakshini M, Enhelling FA, editors. Allelopathy, organisms, processes and applications. Washington: American Chemical Society; 1995. p. 158–66.
Campanella JJ, Olajide AF, Magnus V, Ludwig-Müller J. A novel auxin conjugate hydrolase from wheat with substrate specificity for longer side-chain auxin amide conjugates. Plant Physiol. 2004;135:2230–40. https://doi.org/10.1104/pp.104.043398.
Canher B, Heyman J, Savina M, Devendran A, Eekhout T, Vercauteren I, et al. Rocks in the auxin stream: wound-induced auxin accumulation and ERF115 expression synergistically drive stem cell regeneration. Proc Natl Acad Sci USA. 2020;117:16667–77. https://doi.org/10.1073/pnas.2006620117.
Cano A, Sánchez-García AB, Albacete A, González-Bayón R, Justamante MS, Ibáñez S, et al. Enhanced conjugation of auxin by GH3 enzymes leads to poor adventitious rooting in carnation stem cuttings. Front Plant Sci. 2018;9:566. https://doi.org/10.3389/fpls.2018.00566.
Chhun T, Taketa S, Tsurumi S, Ichii M. Different behaviour of indole-3-acetic acid and indole-3-butyric acid in stimulating lateral root development in rice (Oryza sativa L.). Plant Growth Regul. 2004;43:135–43. https://doi.org/10.1023/B:GROW.0000040120.37448.53.
Chini A, Monte I, Fernández-Barbero G, Boter M, Hicks G, Raikhel N, et al. A small molecule antagonizes jasmonic acid perception and auxin responses in vascular and nonvascular plants. Plant Physiol. 2021;187:1399–413. https://doi.org/10.1093/plphys/kiab369.
Chou J-C, Mulbry WW, Cohen JD. N-Carbobenzyloxy-D-aspartic acid as a competitive inhibitor of indole-3-acetyl-L-aspartic acid hydrolase of Enterobacter agglomerans. Plant Growth Regul. 2002;37:241–8. https://doi.org/10.1023/A:1020872309961.
Ciarkowska A, Ostrowski M, Kozakiewicz A. Biochemical characterization of recombinant UDPG-dependent IAA glucosyltransferase from maize (Zea mays). Int J Mol Sci. 2021;22:3355. https://doi.org/10.3390/ijms22073355.
Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ. Root formation in ethylene-insensitive plants. Plant Physiol. 1999;121:53–60. https://doi.org/10.1104/pp.121.1.53.
Cohen JD, Tang Q, Hegeman AD. Chapter Nine - Using targeted metabolomics to elucidate the indole auxin network in plants. Methods Enzymol. 2022;676:239–78. https://doi.org/10.1016/bs.mie.2022.07.038.
Corrêa LR, Fett-Neto AG. Effects of temperature on adventitious root development in microcuttings of Eucalyptus saligna Smith and Eucalyptus globulus Labill. J Therm Biol. 2004;29:315–24. https://doi.org/10.1016/j.jtherbio.2004.05.006.
Curtis OF. Stimulation of root growth in cuttings by treatment with chemical compounds. New York: Cornell University; 1918.
da Costa CT, de Almeida MR, Ruedell CM, Schwambach J, Maraschin FS, Fett-Neto AG. When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front Plant Sci. 2013;4:133. https://doi.org/10.3389/fpls.2013.00133.
Damodaran S, Strader LC. Indole-3-butyric acid metabolism and transport in Arabidopsis thaliana. Front Plant Sci. 2019;10:851. https://doi.org/10.3389/fpls.2019.00851.
Davies FT, Davis TD, Kester DE. Commercial importance of adventitious rooting to horticulture. In: Davis TD, Haissig BE, editors. Biology of adventitious root formation. Boston: Springer; 1994. p. 53–9.
Davies FT, Geneve RL, Wilson SB. Hartmann and Kester’s plant propagation principles and practices. 9th ed. New York: Pearson; 2018.
Davis W, Endo M, Locke JCW. Spatially specific mechanisms and functions of the plant circadian clock. Plant Physiol. 2022;190:938–51. https://doi.org/10.1093/plphys/kiac236.
De Klerk GJ, Hanecakova J. Ethylene and rooting of mung bean cuttings. The role of auxin induced ethylene synthesis and phase-dependent effects. Plant Growth Regul. 2008;56:203–9. https://doi.org/10.1007/s10725-008-9301-8.
De Almeida MR, Aumond M, Da Costa CT, Schwambach J, Ruedell CM, Correa LR, et al. Environmental control of adventitious rooting in Eucalyptus and Populus cuttings. Trees. 2017;31:1377–90. https://doi.org/10.1007/s00468-017-1550-6.
De Rybel B, Audenaert D, Beeckman T, Kepinski S. The past, present, and future of chemical biology in auxin research. ACS Chem Biol. 2009;4:987–98. https://doi.org/10.1021/cb9001624.
De Rybel B, Audenaert D, Xuan W, Overvoorde P, Strader LC, Kepinski S, et al. A role for the root cap in root branching revealed by the non-auxin probe naxillin. Nat Chem Biol. 2012;8:798–805. https://doi.org/10.1038/nchembio.1044.
Dickinson AJ, Zhang J, Luciano M, Wachsman G, Sandoval E, Schnermann M, et al. A plant lipocalin promotes retinal-mediated oscillatory lateral root initiation. Science. 2021;373:1532–6. https://doi.org/10.1126/science.abf7461.
Dirr M, Heuser CW. The reference manual of woody plant propagation: from seed to tissue culture. 2nd ed. Oregon: Timber Press; 2006.
Druege U, Hilo A, Pérez-Pérez JM, Klopotek Y, Acosta M, Shahinnia F, et al. Molecular and physiological control of adventitious rooting in cuttings: phytohormone action meets resource allocation. Ann Bot. 2019;123:929–49. https://doi.org/10.1093/aob/mcy234.
Einarson B. The manuscripts of Theophrastus’ Historia Plantarum. Class Philol. 1976;71:67–76.
Engvild KC. The chloroindole auxins of pea, strong plant growth hormones or endogenous herbicides? Roskilde: Risø National Laboratory; 1994.
Epstein E, Lavee S. Conversion of indole-3-butyric acid to indole-3-acetic acid by cuttings of grapevine (Vitus vinifera) and olive (Olea europa). Plant Cell Physiol. 1984;25:697–703. https://doi.org/10.1093/oxfordjournals.pcp.a076762.
Epstein E, Ludwig-Müller J. Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. Physiol Plant. 1993;88:382–9. https://doi.org/10.1111/j.1399-3054.1993.tb05513.x.
Epstein E, Wiesman Z. Improved vegetative propagation of olive cultivars with IBA-alanine. Olea. 1987;18:35–8.
Epstein E, Chen KH, Cohen JD. Identification of indole-3-bntyric acid as an endogenous constituent of maize kernels and leaves. Plant Growth Regul. 1989;8:215–23. https://doi.org/10.1007/BF00025391.
Epstein E, Zilkah S, Faingersh G, Rotebaum A. Transport and metabolism of indole-3-butyric acid in easy- and difficult-to-root cuttings of sweet cherry (Prunus avium L.). Acta Hort. 1993;329:292–5. https://doi.org/10.17660/ActaHortic.1993.329.69.
Fallik E, Okon Y, Epstein E, Goldman A, Fischer M. Identification and quantification of IAA and IBA in Azospirillum brasilense-inoculated maize roots. Soil Biol Biochem. 1989;21:147–53. https://doi.org/10.1016/0038-0717(89)90024-2.
Farmer EE, Caldelari D, Pearce G, Walker-Simmons MK, Ryan CA. Diethyldithiocarbamic acid inhibits the octadecanoid signaling pathway for the wound induction of proteinase inhibitors in tomato leaves. Plant Physiol. 1994;106:337–42. https://doi.org/10.1104/pp.106.1.337.
Fattorini L, Falasca G, Kevers C, Rocca LM, Zadra C, Altamura MM. Adventitious rooting is enhanced by methyl jasmonate in tobacco thin cell layers. Planta. 2009;231:155–68. https://doi.org/10.1007/s00425-009-1035-y.
Fattorini L, Veloccia A, Della Rovere F, D’Angeli S, Falasca G, Altamura MM. Indole-3-butyric acid promotes adventitious rooting in Arabidopsis thaliana thin cell layers by conversion into indole-3-acetic acid and stimulation of anthranilate synthase activity. BMC Plant Biol. 2017;17:121. https://doi.org/10.1186/s12870-017-1071-x.
Fattorini L, Hause B, Gutierrez L, Veloccia A, Rovere FD, Piacentini D, et al. Jasmonate promotes auxin-induced adventitious rooting in dark-grown Arabidopsis thaliana seedlings and stem thin cell layers by a cross-talk with ethylene signalling and a modulation of xylogenesis. BMC Plant Biol. 2018;18:182. https://doi.org/10.1186/s12870-018-1392-4.
Fawcett CH, Wain RL, Wightman F. The metabolism of 3-indolealkanecarboxylic acids, and their amides, nitriles and methyl esters in plant tissues. Proc R Soc Lond Ser B. 1960;152:231–54. https://doi.org/10.1098/rspb.1960.0035.
Fogaca CM, Fett-Neto AG. Role of auxin and its modulators in the adventitious rooting of Eucalyptus species differing in recalcitrance. Plant Growth Regul. 2005;45:1–10. https://doi.org/10.1007/s10725-004-6547-7.
Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, et al. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol. 2009;5:344–50. https://doi.org/10.1038/nchembio.161.
Ford YY, Taylor J, Blake P, Marks TR. Gibberellin A3 stimulates adventitious rooting of cuttings from cherry (Prunus avium). Plant Growth Regul. 2002;37:127–33. https://doi.org/10.1023/A:1020584627919.
Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, et al. PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Nat Acad Sci USA. 2011;108:20231–5. https://doi.org/10.1073/pnas.1110682108.
Frick EM, Strader LC. Roles for IBA-derived auxin in plant development. J Exp Bot. 2018;69:169–77. https://doi.org/10.1093/jxb/erx298.
Frigerio M, Alabadí D, Pérez-Gómez J, García-Cárcel L, Phillips AL, Hedden P, et al. Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol. 2006;142:553–63. https://doi.org/10.1104/pp.106.084871.
Fu X, Harberd NP. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature. 2003;421:740–3. https://doi.org/10.1038/nature01387.
Fukui K, Arai K, Tanaka Y, Aoi Y, Kukshal V, Jez JM, et al. Chemical inhibition of the auxin inactivation pathway uncovers the roles of metabolic turnover in auxin homeostasis. Proc Natl Acad Sci USA. 2022;119:e2206869119. https://doi.org/10.1073/pnas.2206869119.
Gogna M, Kumar R, Tiwari LD, Tailor A, Kumari A, Mehta S. Chapter 15 - strigolactones: a new player in regulating adventitious root formation. In: Husen A, editor. Environmental, physiological and chemical controls of adventitious rooting in cuttings. London: Academic; 2022. p. 343–66.
Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci USA. 1998;95:7197–202. https://doi.org/10.1073/pnas.95.12.7197.
Guan L, Tayengwa R, Cheng ZM, Peer WA, Murphy AS, Zhao M. Auxin regulates adventitious root formation in tomato cuttings. BMC Plant Biol. 2019;19:435. https://doi.org/10.1186/s12870-019-2002-9.
Guo K, **a K, Yang ZM. Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide. J Exp Bot. 2008;59:3443–52. https://doi.org/10.1093/jxb/ern194.
Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, et al. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell. 2012;24:2515–27. https://doi.org/10.1105/tpc.112.099119.
Haissig BE. Influences of auxins and auxin synergists on adventitious root primordium initiation and development. NZJ For Sci. 1974;4:311–23.
Haissig BE. Influences of the new auxins 4-carbomethoxyvinylenephenyl indole-3-butyrate and 2,4-dichlorophenyl indole-3-butyrate on adventitious root formation. Can J Bot. 1989;67:2571–5. https://doi.org/10.1139/b89-332.
Halliday KJ, Martínez-García JF, Josse EM. Integration of light and auxin signaling. Cold Spring Harb Perspect Biol. 2009;1:a001586. https://doi.org/10.1101/cshperspect.a001586.
Hamilton RH, Kivilaan A, McManus JM. Biological activity of tetrazole analogues of indole-3-acetic acid and 2,4-dichlorophenoxyacetic acid. Plant Physiol. 1960;35:136–40. https://doi.org/10.1104/pp.35.1.136.
Hanson J. Adventitious root formation induced by gibberellic acid and regulated by the irradiance to the stock plants. Physiol Plant. 1976;36:77–81. https://doi.org/10.1111/j.1399-3054.1976.tb05031.x.
Hayashi KI, Tan X, Zheng N, Hatate T, Kimura Y, Kepinski S, et al. Small-molecule agonists and antagonists of F-box protein–substrate interactions in auxin perception and signaling. Proc Natl Acad Sci USA. 2008;105:5632–7. https://doi.org/10.1073/pnas.0711146105.
Hayashi KI, Arai K, Aoi Y, Tanaka Y, Hira H, Guo R, et al. The main oxidative inactivation pathway of the plant hormone auxin. Nat Commun. 2021;12:6752. https://doi.org/10.1038/s41467-021-27020-1.
He J, **n P, Ma X, Chu J, Wang G. Gibberellin metabolism in flowering plants: an update and perspectives. Front Plant Sci. 2020;11:532. https://doi.org/10.3389/fpls.2020.00532.
Hedden P. Gibberellins. Encyclopedia of applied plant sciences. In: Thomas B, Murphy DJ, Murray BG, editors. Reference module in life science. London: Academic; 2016. p. 411–20.
Hedden P, Phillips AL. Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci. 2000;5:523–30. https://doi.org/10.1016/S1360-1385(00)01790-8.
Heloir MC, Kevers C, Hausman JF, Gaspar T. Changes in the concentrations of auxins and polyamines during rooting of in vitro propagated walnut shoots. Tree Physiol. 1996;16:515–9. https://doi.org/10.1093/treephys/16.5.515.
Hitchcock AE, Zimmerman PW. Comparative activity of root-inducing substances and methods for treating cuttings. J Jpn for Soc. 1939;10:461–80.
Holbrook-Smith D, Toh S, Tsuchiya Y, McCourt P. Small-molecule antagonists of germination of the parasitic plant Striga hermonthica. Nat Chem Biol. 2016;12:724–9. https://doi.org/10.1038/nchembio.2129.
Hu Y, Callebert P, Vandemoortel I, Nguyen L, Audenaert D, Verschraegen L, et al. TR-DB: an open-access database of compounds affecting the ethylene-induced triple response in Arabidopsis. Plant Physiol Biochem. 2014;75:128–37. https://doi.org/10.1016/j.plaphy.2013.12.008.
Huckenpahler BJ. Auxins fail to stimulate rooting of yellow-poplar cuttings. Bot Gaz. 1955;117:73–5. http://www.jstor.org/stable/2473155.
Ito S, Umehara M, Hanada A, Kitahata N, Hayase H, Yamaguchi S, et al. Effects of triazole derivatives on strigolactone levels and growth retardation in rice. PLoS One. 2011;6:e21723. https://doi.org/10.1371/journal.pone.0021723.
Ito S, Umehara M, Hanada A, Yamaguchi S, Asami T. Effects of strigolactone-biosynthesis inhibitor TIS108 on Arabidopsis. Plant Signal Behav. 2013a;8:e24193. https://doi.org/10.4161/psb.24193.
Ito S, Umehara M, Hanada A, Yamaguchi S, Asami T. Tebuconazole derivatives are potent inhibitors of strigolactone biosynthesis. J Pestic Sci. 2013b;38:147–51. https://doi.org/10.1584/jpestics.D13-011.
Ito S, Yamagami D, Umehara M, Hanada A, Yoshida S, Sasaki Y, et al. Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiol. 2017;174:1250–9. https://doi.org/10.1104/pp.17.00301.
Ivanchenko MG, Muday GK, Dubrovsky JG. Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J. 2008;55:335–47. https://doi.org/10.1111/j.1365-313X.2008.03528.x.
Iyer M, Slovin JP, Epstein E, Cohen JD. Transgenic tomato plants with a modified ability to synthesize indole-3-acetyl-β-1-O-D-glucose. J Plant Growth Regul. 2005;24:142–52. https://doi.org/10.1007/s00344-004-0007-5.
Janick J. Horticultural science. 4th ed. New York: W. H. Freeman and Company; 1986.
Jawahir V, Zolman BK. Long chain acyl CoA synthetase 4 catalyzes the first step in peroxisomal indole-3-butyric acid to IAA conversion. Plant Physiol. 2021;185:120–36. https://doi.org/10.1093/plphys/kiaa002.
Jayasinghege CPA, Ozga JA, Nadeau CD, Kaur H, Reinecke DM. TIR1 auxin receptors are implicated in the differential response to 4-Cl-IAA and IAA in develo** pea fruit. J Exp Bot. 2019;70:1239–53. https://doi.org/10.1093/jxb/ery456.
Jez J. Connecting primary and specialized metabolism: Amino acid conjugation of phytohormones by GRETCHEN HAGEN 3 (GH3) acyl acid amido synthetases. Curr Opin Plant Biol. 2022;66:102194. https://doi.org/10.1016/j.pbi.2022.102194.
Jiang K, Asami T. Chemical regulators of plant hormones and their applications in basic research and agriculture. Biosci Biotech Biochem. 2018;82:1265–300. https://doi.org/10.1080/09168451.2018.1462693.
Jiang K, Otani M, Shimotakahara H, Yoon JM, Park SH, Miyaji T, et al. Substituted phthalimide AC94377 is a selective agonist of the gibberellin receptor GID1. Plant Physiol. 2017a;173:825–35. https://doi.org/10.1104/pp.16.00937.
Jiang K, Shimotakahara H, Luo M, Otani M, Nakamura H, Moselhy SS, et al. Chemical screening and development of novel gibberellin mimics. Bioorg Med Chem Lett. 2017b;27:3678–82. https://doi.org/10.1016/j.bmcl.2017.07.012.
Jiang K, Wang J, Ito S, Takahashi I, Ohta T, Murase K, et al. Analysis of the physiological roles and mode of actions of phthalimides as GA signal regulator in rice. J Plant Growth Regul. 2022;42:2637–45. https://doi.org/10.1007/s00344-022-10733-y.
Kamińska M. Role and activity of jasmonates in plants under in vitro conditions. Plant Cell Tiss Organ Cult. 2021;146:425–47. https://doi.org/10.1007/s11240-021-02091-6.
Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, et al. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta. 2011;233:209–16. https://doi.org/10.1007/s00425-010-1310-y.
Katayama M, Masui Y, Kageyama E, Kawabata Y, Kanayama K. Synthesis and biological activities of 4-trifluoromethylindole-3-acetic acid: a new fluorinated indole auxin. Biosci Biotech Biochem. 2008;72:2025–33. https://doi.org/10.1271/bbb.80138.
Kaur N, Reumann S, Hu J. Peroxisome biogenesis and function. Arabidopsis Book. 2009;7:e0123. https://doi.org/10.1199/tab.0123.
Khan N, Hamid FS, Fayaz A, Sabaz AK, Ahmed I, Muhammad AK, et al. Optimization of IBA concentration for rapid initiation of roots and ultimate growth of kiwi seedlings and the association between root system architecture and seedlings growth. Pak J Agric Res. 2020;33:63–71. https://doi.org/10.17582/journal.pjar/2020/33.1.63.71.
Kim H, Cha HC. Effect of gibberellin on the adventitious root formation from the leaves-derived calli in Persicaria perfoliata. J Life Sci. 2015;25:390–6. https://doi.org/10.5352/JLS.2015.25.4.390.
Kim HJ, Lynch JP, Brown KM. Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant Cell Environ. 2008;31:1744–55. https://doi.org/10.1111/j.1365-3040.2008.01886.x.
King RW, Moritz T, Evans LT, Junttila O, Herlt AJ. Long-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex. Plant Physiol. 2001;127:624–32. https://doi.org/10.1104/pp.010378.
Klopotek Y, Haensch KT, Hause B, Hajirezaei MR, Druege U. Dark exposure of petunia cuttings strongly improves adventitious root formation and enhances carbohydrate availability during rooting in the light. J Plant Physiol. 2010;167:547–54. https://doi.org/10.1016/j.jplph.2009.11.008.
Konjoian P. Nursery Management: basic principles of nursery crop propagation. 2017. https://www.nurserymag.com/news/grow-tech-basic-principles-nursery-crop-propagation/. Accessed 1 Dec 2023.
Kreiser M, Giblin C, Murphy R, Fiesel P, Braun L, Johnson G, et al. Conversion of indole-3-butyric acid to indole-3-acetic acid in shoot tissue of hazelnut (Corylus) and elm (Ulmus). J Plant Growth Regul. 2016;35:710–21. https://doi.org/10.1007/s00344-016-9574-5.
Lakehal A, Bellini C. Control of adventitious root formation: insights into synergistic and antagonistic hormonal interactions. Physiol Plant. 2019;165:90–100. https://doi.org/10.1111/ppl.12823.
Lakehal A, Dob A, Novák O, Bellini C. A DAO1-mediated circuit controls auxin and jasmonate crosstalk robustness during adventitious root initiation in Arabidopsis. Int J Mol Sci. 2019;20:4428. https://doi.org/10.3390/ijms20184428.
LaRue CD. The effects of wounding and wound hormones on root formation. Proc Natl Acad Sci USA. 1941;27:388–92. https://doi.org/10.1073/pnas.27.8.388.
Lau OL, Yang SF. Inhibition of ethylene production by cobaltous ion. Plant Physiol. 1976;58:114–7. https://doi.org/10.1104/pp.58.1.114.
Le Deunff E, Beauclair P, Deleu C, Lecourt J. Inhibition of aminotransferases by aminoethoxyvinylglycine triggers a nitrogen limitation condition and deregulation of histidine homeostasis that impact root and shoot development and nitrate uptake. Front Plant Sci. 2019;10:1387. https://doi.org/10.3389/fpls.2019.01387.
Lee TT, Starratt AN. Inhibition of conjugation of indole-3-acetic acid with amino acids by 2,6-dihydroxyacetophenone in Teucrium canadense. Phytochemistry. 1986;25:2457–61. https://doi.org/10.1016/S0031-9422(00)84488-X.
Li SW. Molecular bases for the regulation of adventitious root generation in plants. Front Plant Sci. 2021;12:614072. https://doi.org/10.3389/fpls.2021.614072.
Li G, Zhu C, Gan L, Ng D, **a K. GA3 enhances root responsiveness to exogenous IAA by modulating auxin transport and signalling in Arabidopsis. Plant Cell Rep. 2015;34:483–94. https://doi.org/10.1007/s00299-014-1728-y.
Li W, Lacey RF, Ye Y, Lu J, Yeh KC, **ao Y, et al. Triplin, a small molecule, reveals copper ion transport in ethylene signaling from ATX1 to RAN1. PLoS Genet. 2017;13:e1006703. https://doi.org/10.1371/journal.pgen.1006703.
Li Y, Qiu L, Zhang Q, Zhuansun X, Li H, Chen X, et al. Exogenous sodium diethyldithiocarbamate, a jasmonic acid biosynthesis inhibitor, induced resistance to powdery mildew in wheat. Plant Direct. 2020;4:e00212. https://doi.org/10.1002/pld3.212.
Lin S, Ye M, Li X, **ng Y, Liu M, Zhang J, et al. A novel inhibitor of the jasmonic acid signaling pathway represses herbivore resistance in tea plants. Hortic Res. 2022;9:uhab038. https://doi.org/10.1093/hr/uhab038.
Liu X, Barkawi L, Gardner G, Cohen JD. Transport of indole-3-butyric acid and indole-3-acetic acid in Arabidopsis hypocotyls using stable isotope labeling. Plant Physiol. 2012;158:1988–2000. https://doi.org/10.1104/pp.111.191288.
Ludwig-Müller J. Indole-3-butyric acid synthesis in ecotypes and mutants of Arabidopsis thaliana under different growth conditions. J Plant Physiol. 2007;164:47–59. https://doi.org/10.1016/j.jplph.2005.10.008.
Ludwig-Müller J. Synthesis and hydrolysis of auxins and their conjugates with different side-chain lengths: are all products active auxins? Period Biol. 2020;121–122(3–4):81–96. https://doi.org/10.18054/pb.v121-122i3-4.10516.
Ludwig-Müller J, Epstein E. Occurrence and in vivo biosynthesis of indole-3-butyric acid in corn (Zea mays L.). Plant Physiol. 1991;97:765–70. https://doi.org/10.1104/pp.97.2.765.
Ludwig-Müller J, Sass S, Sutter EG, Wodner M, Epstein E. Indole-3-butyric acid in Arabidopsis thaliana. I. Identification and quantification. Plant Growth Regul. 1993;13:179–87. https://doi.org/10.1007/BF00024260.
Ludwig-Müller J, Vertocnik A, Town CD. Analysis of indole-3-butyric acid-induced adventitious root formation on Arabidopsis stem segments. J Exp Bot. 2005;56:2095–105. https://doi.org/10.1093/jxb/eri208.
Magnus V, Ozga JA, Reinecke DM, Pierson GL, LaRue TA, Cohen JD, et al. 4-Chloroindole-3-acetic and indole-3-acetic acids in fruits and roots of Pisum sativum. Phytochemistry. 1997;46:675–81. https://doi.org/10.1016/S0031-9422(97)00229-X.
Maki Y, Soejima H, Sugiyama T, Sato T, Yamaguchi J, Watahiki MK. Conjugates of 3-phenyllactic acid and tryptophan enhance root-promoting activity without adverse effects in Vigna angularis. Plant Biotechnol. 2022;39:173–7. https://doi.org/10.5511/plantbiotechnology.21.1217a.
Marston ME. The history of plant propagation in England by vegetative methods not requiring the use of a root-stock. Sci Hort. 1955;12:118–32. http://www.jstor.org/stable/45126088.
Marumo S, Kato, Y, Nitani F. JPH03169858A New indolebutyric acid derivative. 1991. https://worldwide.espacenet.com/patent/search/family/017971286/publication/JPH03169858A?q=NEW%20INDOLEBUTYRIC%20ACID%20DERIVATIVE. Accessed 5 Dec 2023.
Mashita O, Koishihara H, Fukui K, Nakamura H, Asami T. Discovery and identification of 2-methoxy-1-naphthaldehyde as a novel strigolactone-signaling inhibitor. J Pestic Sci. 2016;41:71–8. https://doi.org/10.1584/jpestics.D16-028.
Matosevich R, Cohen I, Gil-Yarom N, Modrego A, Friedlander-Shani L, Verna C, et al. Local auxin biosynthesis is required for root regeneration after wounding. Nat Plants. 2020;6:1020–30. https://doi.org/10.1038/s41477-020-0737-9.
Mauriat M, Petterle A, Bellini C, Moritz T. Gibberellins inhibit adventitious rooting in hybrid aspen and Arabidopsis by affecting auxin transport. Plant J. 2014;78:372–84. https://doi.org/10.1111/tpj.12478.
Mazzoni-Putman SM, Brumos J, Zhao C, Alonso JM, Stepanova AN. Auxin interactions with other hormones in plant development. Cold Spring Harb Perspect Biol. 2021;13:a039990. https://doi.org/10.1101/cshperspect.a039990.
McDaniel B, Binder BM. Ethylene Receptor1 (ETR1) is sufficient and has the predominant role in mediating inhibition of ethylene responses by silver in Arabidopsis thaliana. J Biol Chem. 2012;287:26094–103. https://doi.org/10.1074/jbc.M112.383034.
Meesters C, Mönig T, Oeljeklaus J, Krahn D, Westfall CS, Hause B, et al. A chemical inhibitor of jasmonate signaling targets JAR1 in Arabidopsis thaliana. Nat Chem Biol. 2014;10:830–6. https://doi.org/10.1038/nchembio.1591.
Michniewicz M, Powers SK, Strader LC. IBA transport by PDR proteins. In: Geisler M, editor. Plant ABC transporters. Cham: Springer; 2014. p. 313–31.
Michniewicz M, Ho CH, Enders TA, Floro E, Damodaran S, Gunther LK, et al. TRANSPORTER OF IBA1 Links auxin and cytokinin to influence root architecture. Dev Cell. 2019;50:599–609.e4. https://doi.org/10.1016/j.devcel.2019.06.010.
Mihaljević S, Salopek-Sondi B. Alanine conjugate of indole-3-butyric acid improves rooting of highbush blueberries. Plant Soil Environ. 2012;58:236–41. https://doi.org/10.17221/34/2012-PSE.
Miller BM, Bassuk NL. Gibberellic acid 4+7 influences shoot growth of seedling pecan and bitternut hickory. J Environ Hort. 2022;40:39–45. https://doi.org/10.24266/2573-5586-40.2.45.
Miyazaki S, Jiang K, Kobayashi M, Asami T, Nakajima M. Helminthosporic acid functions as an agonist for gibberellin receptor. Biosci Biotechnol Biochem. 2017;81:2152–9. https://doi.org/10.1080/09168451.2017.1381018.
Miyazaki S, Tomita K, Yamane H, Kobayashi M, Asami T, Nakajima M. Characterization of a helminthosporic acid analog that is a selective agonist of gibberellin receptor. Bioorg Med Chem Lett. 2018;28:2465–70. https://doi.org/10.1016/j.bmcl.2018.06.005.
Monte I, Hamberg M, Chini A, Gimenez-Ibanez S, García-Casado G, Porzel A, et al. Rational design of a ligand-based antagonist of jasmonate perception. Nat Chem Biol. 2014;10:671–6. https://doi.org/10.1038/nchembio.1575.
Monte I, Caballero J, Zamarreño AM, Fernández-Barbero G, García-Mina JM, Solano R. JAZ is essential for ligand specificity of the COI1/JAZ co-receptor. Proc Natl Acad Sci USA. 2022;119:e2212155119. https://doi.org/10.1073/pnas.2212155119.
Monteuuis O, Bon MC. Influence of auxins and darkness on in vitro rooting of micropropagated shoots from mature and juvenile Acacia mangium. Plant Cell Tissue Organ Cult. 2000;63:173–7. https://doi.org/10.1023/A:1010611126950.
Morffy N, Strader LC. Structural aspects of auxin signaling. Cold Spring Harb Perspect Biol. 2022;14:a039883. https://doi.org/10.1101/cshperspect.a039883.
Mosblech A, Thurow C, Gatz C, Feussner I, Heilmann I. Jasmonic acid perception by COI1 involves inositol polyphosphates in Arabidopsis thaliana. Plant J. 2011;65:949–57. https://doi.org/10.1111/j.1365-313X.2011.04480.x.
Moura-Costa PH, Lundoh L. The effects of auxins (IAA, NAA AND 2,4-D) on rooting of Dryobalanops Lanceolata (Kapur - Dipterocarpaceae) cuttings. J Trop For Sci. 1994;7:338–40. http://www.jstor.org/stable/43581821.
Negi S, Ivanchenko MG, Muday GK. Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J. 2008;55:175–87. https://doi.org/10.1111/j.1365-313X.2008.03495.x.
Negi S, Sukumar P, Liu X, Cohen JD, Muday GK. Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J. 2010;61:3–15. https://doi.org/10.1111/j.1365-313X.2009.04027.x.
Nordström AC, Jacobs FA, Eliasson L. Effect of exogenous indole-3-acetic acid and indole-3-butyric acid on internal levels of the respective auxins and their conjugation with aspartic acid during adventitious root formation in pea cuttings. Plant Physiol. 1991;96:856–61. https://doi.org/10.1104/pp.96.3.856.
Novak O, Henykova E, Sairanen I, Kowalczyk M, Pospisil T, Ljung K. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 2012;72:523–36. https://doi.org/10.1111/j.1365-313X.2012.05085.x.
Oh K, Hoshi T, Tomio S, Ueda K, Hara K. A chemical genetics strategy that identifies small molecules which induce the triple response in Arabidopsis. Molecules. 2017;22:2270. https://doi.org/10.3390/molecules22122270.
Owens LD, Lieberman M, Kunishi A. Inhibition of ethylene production by rhizobitoxine. Plant Physiol. 1971;48:1–4. https://doi.org/10.1104/pp.48.1.1.
Pacurar DI, Perrone I, Bellini C. Auxin is a central player in the hormone cross-talks that control adventitious rooting. Physiol Plant. 2014;151:83–96. https://doi.org/10.1111/ppl.12171.
Pan R, Tian X. Comparative effect of IBA, BSAA and 5,6-Cl2-IAA-Me on the rooting of hypocotyl in mung bean. Plant Growth Regul. 1999;27:91–8. https://doi.org/10.1023/A:1006154426941.
Pan R, Liu J, Wang S, Hu J. Peroxisomes: versatile organelles with diverse roles in plants. New Phytol. 2020;225:1410–27. https://doi.org/10.1111/nph.16134.
Pan X, Yang Z, Xu L. Dual roles of jasmonate in adventitious rooting. J Exp Bot. 2021;72:6808–10. https://doi.org/10.1093/jxb/erab378.
Park SH, Elhiti M, Wang H, Xu A, Brown D, Wang A. Adventitious root formation of in vitro peach shoots is regulated by auxin and ethylene. Sci Hort. 2017;226:250–60. https://doi.org/10.1016/j.scienta.2017.08.053.
Peiter E. The plant vacuole: emitter and receiver of calcium signals. Cell Calcium. 2011;50:120–8. https://doi.org/10.1016/j.ceca.2011.02.002.
Pérez-Henríquez P, Raikhel NV, Norambuena L. Endocytic trafficking towards the vacuole plays a key role in the auxin receptor SCFTIR-independent mechanism of lateral root formation in A. thaliana. Mol Plant. 2012;5:1195–209. https://doi.org/10.1093/mp/sss066.
Pincelli-Souza RP, Sousa Moreira L, Cohen JD. Improvements for the micropropagation of hybrid hazelnut (C. Americana x C. avellana). Horticulturae. 2022;8:849. https://doi.org/10.3390/horticulturae8090849.
Pirrung MC, Bleecker AB, Inoue Y, Rodriguez FI, Sugawara N, Wada T, et al. Ethylene receptor antagonists: strained alkenes are necessary but not sufficient. Chem Biol. 2008;15:313–21. https://doi.org/10.1016/j.chembiol.2008.02.018.
Pizarro A, Díaz-Sala C. Effect of polar auxin transport and gibberellins on xylem formation in pine cuttings under adventitious rooting conditions. Israel J Plant Sci. 2020;67(1–2):27–39. https://doi.org/10.1163/22238980-20191120.
Poirier Y, Ventre G, Caldelari D. Increased flow of fatty acids toward beta-oxidation in develo** seeds of Arabidopsis deficient in diacylglycerol acyltransferase activity or synthesizing medium-chain-length fatty acids. Plant Physiol. 1999;121:1359–66. https://doi.org/10.1104/pp.121.4.1359.
Preece JE. A century of progress with vegetative plant propagation. HortScience. 2003;38:1015–25. https://doi.org/10.21273/HORTSCI.38.5.1015.
Qin H, He L, Huang R. The coordination of ethylene and other hormones in primary root development. Front Plant Sci. 2019;10:874. https://doi.org/10.3389/fpls.2019.00874.
Quareshy M, Prusinska J, Kieffer M, Fukui K, Pardal AJ, Lehmann S, et al. The tetrazole analogue of the auxin indole-3-acetic acid binds preferentially to TIR1 and not AFB5. ACS Chem Biol. 2018;13:2585–94. https://doi.org/10.1021/acschembio.8b00527.
Rademacher W. Growth Retardants: effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol. 2000;51:501–31. https://doi.org/10.1146/annurev.arplant.51.1.501.
Rashotte AM, Poupart J, Waddell CS, Muday GK. Transport of the two natural auxins, indole-3-butyric acid and indole-3-acetic acid, in Arabidopsis. Plant Physiol. 2003;133:761–72. https://doi.org/10.1104/pp.103.022582.
Rayle DL, Evans ML, Hertel R. Action of auxin on cell elongation. Proc Natl Acad Sci USA. 1970;65:184–91. https://doi.org/10.1073/pnas.65.1.184.
Reumann S, Bartel B. Plant peroxisomes: recent discoveries in functional complexity, organelle homeostasis, and morphological dynamics. Curr Opin Plant Biol. 2016;34:17–26. https://doi.org/10.1016/j.pbi.2016.07.008.
Richter R, Behringer C, Zourelidou M, Schwechheimer C. Convergence of auxin and gibberellin signaling on the regulation of the GATA transcription factors GNC and GNL in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2013;110:13192–7. https://doi.org/10.1073/pnas.1304250110.
Rinaldi MA, Patel AB, Park J, Lee K, Strader LC, Bartel B. The roles of β-oxidation and cofactor homeostasis in peroxisome distribution and function in Arabidopsis thaliana. Genetics. 2016;204:1089–115. https://doi.org/10.1534/genetics.116.193169.
Riov J. Endogenous and exogenous auxin conjugates in rooting of cuttings. Acta Hort. 1993;329:284–8. https://doi.org/10.17660/ActaHortic.1993.329.67.
Riov J, Fox H, Attias R, Shklar G, Farkash-Haim L, Sitbon R, et al. Improved method for vegetative propagation of mature Pinus halepensis and its hybrids by cuttings. Israel J Plant Sci. 2020;67(1–2):5–15. https://doi.org/10.1163/22238980-20191118.
Rodríguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB. A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science. 1999;283:996–8. https://doi.org/10.1126/science.283.5404.996.
Roth O, Yechezkel S, Serero O, Eliyahu A, Vints I, Tzeela P, et al. Slow release of a synthetic auxin induces formation of adventitious roots in recalcitrant woody plants. Nat Biotechnol. 2024. https://doi.org/10.1038/s41587-023-02065-3.
Roussos PA. Adventitious root formation in plants: the implication of hydrogen peroxide and nitric oxide. Antioxidants. 2023;12:862. https://doi.org/10.3390/antiox12040862.
Růzicka K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, et al. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell. 2007;19:2197–212. https://doi.org/10.1105/tpc.107.052126.
Salope-Sondi B, Pollmann S, Gruden K, Oelmüller R, Ludwig-Müller J. Improvement of root architecture under abiotic stress through control of auxin homeostasis in Arabidopsis and Brassica crops. Endocyt Cell Res. 2015;26:100–11. http://www.journals4free.com/link.jsp?l=16699202.
Satoh S, Esashi Y. α-Aminoisobutyric acid: a probable competitive inhibitor of conversion of 1-aminocyclopropane-1-carboxylic acid to ethylene. Plant Cell Physiol. 1980;21:939–49. https://doi.org/10.1093/oxfordjournals.pcp.a076082.
Schaller GE, Binder BM. Inhibitors of ethylene biosynthesis and signaling. In: Binder BM, Schaller GE, editors. Ethylene signaling. New York: Humana Press; 2017. p. 223–35.
Schenck D, Christian M, Jones A, Lüthen H. Rapid auxin-induced cell expansion and gene expression: a four-decade-old question revisited. Plant Physiol. 2010;152:1183–5. https://doi.org/10.1104/pp.109.149591.
Schlicht M, Ludwig-Müller J, Burbach C, Volkmann D, Baluska F. Indole-3-butyric acid induces lateral root formation via peroxisome-derived indole-3-acetic acid and nitric oxide. New Phytol. 2013;200:473–82. https://doi.org/10.1111/nph.12377.
Schneider EA, Kazakoff CW, Wightman F. Gas chromatography-mass spectrometry evidence for several endogenous auxins in pea seedlings organs. Planta. 1985;165:232–41. https://doi.org/10.1007/BF00395046.
Sergeant MJ, Li JJ, Fox C, Brookbank N, Rea D, Bugg TD, et al. Selective inhibition of carotenoid cleavage dioxygenases. J Biol Chem. 2009;284:5257–64. https://doi.org/10.1074/jbc.M805453200.
Sharma K, Thapa T. The various methods used for the clonal propagation in horticultural crops: a review. Agric Rev. 2022;43:229–33. https://doi.org/10.18805/ag.R-2136.
Shechter S, Goldschmidt EE, Galili D. Persistence of [14C] gibberellin A3 and [3H] gibberellin A1 in senescing, ethylene treated citrus and tomato fruit. Plant Growth Regul. 1989;8:243–53. https://doi.org/10.1007/BF00025394.
Sherp AM, Westfall CS, Alvarez S, Jez JM. Arabidopsis thaliana GH3.15 acyl acid amido synthetase has a highly specific substrate preference for the auxin precursor indole-3-butyric acid. J Biol Chem. 2018;293:4277–88. https://doi.org/10.1074/jbc.RA118.002006.
Simon S, Kubeš M, Baster P, Robert S, Dobrev PI, Friml J, et al. Defining the selectivity of processes along the auxin response chain: a study using auxin analogues. New Phytol. 2013;200:1034–48. https://doi.org/10.1111/nph.12437.
Šípošová K, Kollárová K, Lišková D, Vivodová Z. The effects of IBA on the composition of maize root cell walls. J Plant Physiol. 2019;239:10–7. https://doi.org/10.1016/j.jplph.2019.04.004.
Slovin JP. Phytotoxic conjugates of indole-3-acetic acid: potential agents for biochemical selection of mutants in conjugate hydrolysis. Plant Growth Regul. 1997;21:215–21. https://doi.org/10.1023/A:1005873123184.
Slovin JP, Bandurski RS, Cohen JD. Auxin. In: Hooykaas PJJ, Hall MA, Libbenga KR, editors. Biochemistry and molecular biology of plant hormones. Amsterdam: Elsevier; 1999. p. 115–40.
Song P, Xu H, Zhang J, Chen H, Li L, Qu Y, et al. Functional analysis of indole-3-hexanoic acid as a novel auxin from Arabidopsis thaliana. Planta. 2021;254:69. https://doi.org/10.1007/s00425-021-03719-9.
Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, Geiss G, et al. Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell. 2005;17:1343–59. https://doi.org/10.1007/s00425-021-03719-910.1105/tpc.105.031625.
Spiess GM, Zolman BK. Peroxisomes as a source of auxin signaling molecules. In: del Río L, editor. Peroxisomes and their key role in cellular signaling and metabolism. Subcellular biochemistry. Dordrecht: Springer; 2013. p. 115–40.
Staswick PE. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol. 2009;150:1310–21. https://doi.org/10.1104/pp.109.138529.
Steffens B, Rasmussen A. The physiology of adventitious roots. Plant Physiol. 2016;170:603–17. https://doi.org/10.1104/pp.15.01360.
Stepanova AN, Yun J, Likhacheva AV, Alonso JM. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell. 2007;19:2169–85. https://doi.org/10.1105/tpc.107.052068.
Stokes CE, Bassuk NL, Miller BM. Light reduction, banding, and IBA treatments influence adventitious rooting of Lindera benzoin stem cuttings. HortScience. 2023;58:506–12. https://doi.org/10.21273/HORTSCI17022-22.
Strader LC, Beisner ER, Bartel B. Silver ions increase auxin efflux independently of effects on ethylene response. Plant Cell. 2009;21:3585–90. https://doi.org/10.1105/tpc.108.065185.
Strader LC, Chen GL, Bartel B. Ethylene directs auxin to control root cell expansion. Plant J. 2010a;64:874–84. https://doi.org/10.1111/j.1365-313X.2010.04373.x.
Strader LC, Culler AH, Cohen JD, Bartel B. Conversion of endogenous indole-3-butyric acid to indole-3-acetic acid drives cell expansion in Arabidopsis seedlings. Plant Physiol. 2010b;153:1577–86. https://doi.org/10.1104/pp.110.157461.
Strader LC, Wheeler DL, Christensen SE, Berens JC, Cohen JD, Rampey RA, et al. Multiple facets of Arabidopsis seedling development require indole-3-butyric acid-derived auxin. Plant Cell. 2011;23:984–99. https://doi.org/10.1105/tpc.111.083071.
Struve DK, Arnold MA. Aryl esters of indolebutyric acid increase root regeneration in 3–0 red oak seedlings. Can J Forest Res. 1986a;16:673–5. https://doi.org/10.1139/x86-119.
Struve DK, Arnold MA. Aryl esters of IBA increase rooted cutting quality of red maple ‘Red Sunset’ softwood cuttings. HortScience. 1986b;21:1392–3. https://doi.org/10.21273/HORTSCI.21.6.1392.
Struve DK, Rhodus WT. Phenyl indole-3-thiolobutyrate increases growth of transplanted 1–0 red oak. Can J Forest Res. 1988;18:131–4. https://doi.org/10.1139/x88-020.
Sukiran NA, Pollastri S, Steel PG, Knight MR. Plant growth promotion by the interaction of a novel synthetic small molecule with GA-DELLA function. Plant Direct. 2022;6:e398. https://doi.org/10.1002/pld3.398.
Sunayana M, Sasikala C, Ramana C. Rhodestrin: a novel indole terpenoid phytohormone from Rhodobacter sphaeroides. Biotechnol Lett. 2005;27:1897–900. https://doi.org/10.1007/s10529-005-3900-5.
Szerszen JB, Szczyglowski K, Bandurski RS. Iaglu, a gene from Zea mays involved in conjugation of growth hormone indole-3-acetic acid. Science. 1994;265:1699–701. https://doi.org/10.1126/science.8085154.
Tanakh. Tanakh: a new translation of the holy scriptures according to the traditional Hebrew text. Philadelphia: Jewish Publication Society; 1985.
Taylor BD, Hoover BK. Foliar auxin application improves adventitious rooting of wall germander cuttings. HortTechnology. 2018;28:17–21. https://doi.org/10.21273/HORTTECH03891-17.
Thimann KV, Went FW. On the chemical nature of the root-forming hormone. Proc Kon Akad Wetensch (Amsterdam). 1934;37:456–8. https://www.cabidigitallibrary.org/doi/full/10.5555/19350700467. Accessed 4 Dec 2023.
Thimann KV, Behnke-Rogers J. The use of auxins in the rooting of woody cuttings. Petersham: Harvard Forest; 1950.
Thimann KV, Koepfli JB. Identity of the growth-promoting and root-forming substances of plants. Nature. 1935;135:101–2. https://doi.org/10.1038/135101a0.
Tillmann MA, Tang Q, Cohen JD. Protocol: Analytical methods for visualizing the indolic precursor network leading to auxin biosynthesis. Plant Methods. 2021;17:63. https://doi.org/10.1186/s13007-021-00763-0.
Tillmann MA, Tang Q, Gardner G, Cohen JD. Complexity of the auxin biosynthetic network in Arabidopsis hypocotyls is revealed by multiple stable-labeled precursors. Phytochemistry. 2022;200:113219. https://doi.org/10.1016/j.phytochem.2022.1132192022.
Uzunova VV, Quareshy M, Del Genio CI, Napier RM. Tomographic docking suggests the mechanism of auxin receptor TIR1 selectivity. Open Biol. 2016;6:160139. https://doi.org/10.1098/rsob.160139.
Vadassery J, Ballhorn DJ, Fleming SR, Mazars C, Pandey SP, Schmidt A, et al. Neomycin: an effective inhibitor of jasmonate-induced reactions in plants. J Plant Growth Regul. 2019;38:713–22. https://doi.org/10.1007/s00344-018-9884-x.
Vaičiukynė M, Žiauka J, Žūkienė R, Vertelkaitė L, Kuusienė S. Abscisic acid promotes root system development in birch tissue culture: a comparison to aspen culture and conventional rooting-related growth regulators. Physiol Plant. 2019;165:114–22. https://doi.org/10.1111/ppl.12860.
Van der Krieken WM, Breteler H, Visser MHM. The effect of the conversion of indolebutyric acid into indoleacetic acid on root formation on microcuttings of Malus. Plant Cell Physiol. 1992;33:709–13. https://doi.org/10.1093/oxfordjournals.pcp.a078309.
Van der Krieken WM, Breteler H, Visser MHM, Mavridou D. The role of the conversion of IBA into IAA on root regeneration in apple: introduction of a test system. Plant Cell Rep. 1993;12:203–6. https://doi.org/10.1007/BF00237054.
Van der Krieken WM, Kodde J, Visser MHM, Blaakmeer A, de Groot K, Leegstra L, Tsardakas D. Increased induction of adventitious rooting by slow release auxins and elicitors. In: Altman A, Waisel Y, editors. Biology of root formation and development. Boston: Springer; 1997. p. 95–104.
Veloccia A, Fattorini L, Della Rovere F, Sofo A, D’Angeli S, Betti C, et al. Ethylene and auxin interaction in the control of adventitious rooting in Arabidopsis thaliana. J Exp Bot. 2016;67:6445–58. https://doi.org/10.1093/jxb/erw415.
Verstraeten I, Beeckman T, Geelen D. Adventitious root induction in Arabidopsis thaliana as a model for in vitro root organogenesis. In: De Smet I, editor. Plant Organogenesis. Totowa: Humana Press; 2013. p. 159–75.
Visser EJW, Cohen JD, Barendse GWM, Blom CWPM, Voesenek LACJ. An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm. Plant Physiol. 1996;112:1687–92. https://doi.org/10.1104/pp.112.4.1687.
Voß U, Wilson MH, Kenobi K, Gould PD, Robertson FC, Peer WA, et al. The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat Commun. 2015;6:7641. https://doi.org/10.1038/ncomms8641.
Wang S, Taketa S, Ichii M, Xu L, **a K, Zhou X. Lateral root formation in rice (Oryza Sativa L.): differential effects of indole-3-acetic acid and indole-3-butyric acid. Plant Growth Regul. 2003;41:41–7. https://doi.org/10.1023/A:1027384528993143.
Warmund MR, Trinklein DH, Ellersieck MR, Smeda RJ. Antitranspirants partially mitigate auxin herbicide injury on tomato plants. HortScience. 2021;56:932–9. https://doi.org/10.21273/HORTSCI15888-21.
Wasternack C, Song S. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot. 2017;68:1303–21. https://doi.org/10.1093/jxb/erw443.
Weaver RJ. Plant growth substances in agriculture. San Francisco: W.H. Freeman; 1972.
Weiss E. “Beginnings of fruit growing in the old world”–two generations later. Israel J Plant Sci. 2015;62:75–85. https://doi.org/10.1080/07929978.2015.1007718.
Went FW. On a substance causing root formation. Proc Kon Akad Wetensch, Amsterdam. 1929;32:35–9.
Wiesman Z, Riov J, Epstein E. Characterization and rooting ability of indole-3-butyric acid conjugates formed during rooting of mung bean cuttings. Plant Physiol. 1989;91:1080–4. https://doi.org/10.1104/pp.91.3.1080.
Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C. Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell. 2011;23:2184–95. https://doi.org/10.1105/tpc.111.086355.
Woodward AW, Bartel B. Auxin: regulation, action, and interaction. Ann Bot. 2005;95:707–35. https://doi.org/10.1093/aob/mci083.
**ang H, Yao R, Quan T, Wang F, Chen L, Du X, et al. Simple β-lactones are potent irreversible antagonists for strigolactone receptors. Cell Res. 2017;25:1525–8. https://doi.org/10.1038/cr.2017.105.
**e Y, Zhu Y, Wang N, Luo M, Ota T, Guo R, et al. Chemical genetic screening identifies nalacin as an inhibitor of GH3 amido synthetase for auxin conjugation. Proc Natl Acad Sci USA. 2022;119:e2209256119. https://doi.org/10.1073/pnas.2209256119.
Xuan W, Xu S, Yuan X, Shen W. Carbon monoxide: a novel and pivotal signal molecule in plants? Plant Signal Behav. 2008;3:381–2. https://doi.org/10.4161/psb.3.6.5374.
Yao R, Wang F, Ming Z, Du X, Chen L, Wang Y, et al. ShHTL7 is a noncanonical receptor for strigolactones in root parasitic weeds. Cell Res. 2017;27:838–41. https://doi.org/10.1038/cr.2017.3.
Yoon JM, Nakajima M, Mashiguchi K, Park SH, Otani M, Asami T. Chemical screening of an inhibitor for gibberellin receptors based on a yeast two-hybrid system. Bioorg Med Chem Lett. 2013;23:1096–8. https://doi.org/10.1016/j.bmcl.2012.12.007.
Yoshihara T, Greulich F. Biosynthesis of jasmonoids and their functions. In: Barton SD, Nakanishi K, Meth-Cohn O, editors. Comprehensive natural products chemistry. London: Pergamon; 1999. p. 117–38.
Yu X, Cui X, Wu C, Shi S, Yan S. Salicylic acid inhibits gibberellin signaling through receptor interactions. Mol Plant. 2022;15:1759–71. https://doi.org/10.1016/j.molp.2022.10.001.
Zelená E, Fuksová K. The effect of indole-3-acetylaspartic acid on adventitious root formation on bean cuttings. Plant Growth Regul. 1991;10:73–8.
Zemlyanskaya EV, Omelyanchuk NA, Ubogoeva EV, Mironova VV. Deciphering auxin-ethylene crosstalk at a systems level. Int J Mol Sci. 2018;19:4060. https://doi.org/10.3390/ijms19124060.
Zhang W, Fan J, Tan Q, Zhao M, Zhou T, Cao F. The effects of exogenous hormones on rooting process and the activities of key enzymes of Malus hupehensis stem cuttings. PLoS One. 2017;12:e0172320. https://doi.org/10.1371/journal.pone.0172320.
Zhang J, Zhou T, Zhang C, Zheng W, Li J, Jiang W, et al. Gibberellin disturbs the balance of endogenesis hormones and inhibits adventitious root development of Pseudostellaria heterophylla through regulating gene expression related to hormone synthesis. Saudi J Biol Sci. 2021;28:135–47. https://doi.org/10.1016/j.sjbs.2020.09.022.
Zhao Y, Chen Y, Jiang C, Lu MZ, Zhang J. Exogenous hormones supplementation improve adventitious root formation in woody plants. Front Bioeng Biotechnol. 2022;10:1009531. https://doi.org/10.3389/fbioe.2022.1009531.
Zheng Z, Guo Y, Novák O, Dai X, Zhao Y, Ljung K, et al. Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nat Chem Biol. 2013;9:244–6. https://doi.org/10.1038/nchembio.1178.
Zhou R, Yu M, Pharis RP. 16,17-dihydro gibberellin A5 competitively inhibits a recombinant Arabidopsis GA 3beta-hydroxylase encoded by the GA4 gene. Plant Physiol. 2004;135:1000–7. https://doi.org/10.1104/pp.104.041509.
Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, et al. A jasmonate signaling network activates root stem cells and promotes regeneration. Cell. 2019;177:942.e14–956e.14. https://doi.org/10.1016/j.cell.2019.03.006.
Žiauka J, Kuusienė S. Different inhibitors of the gibberellin biosynthesis pathway elicit varied responses during in vitro culture of aspen (Populus tremula L.). Plant Cell Tissue Organ Cult. 2010;102:221–8. https://doi.org/10.1007/s11240-010-9725-5.
Zimmerman PW, Crocker W, Hitchcock AE. Initiation and stimulation of roots from exposure of plants to carbon monoxide. Contrib Boyce Thompson Inst. 1933;5:1–17.
Zimmerman PW, Hitchcock AE. Experiments with vapors and solutions of growth substances. Contrib Boyce Thompson Inst. 1939;10:481–508.
Zimmerman PW, Wilcoxon F. Several chemical growth substances which cause initiation of roots and other responses in plants. Contrib Boyce Thompson Inst. 1935;7:209–29.
Zohary D, Spiegel-Roy P. Beginnings of fruit growing in the Old World: olive, grape, date, and fig emerge as important Bronze Age additions to grain agriculture in the Near East. Science. 1975;187:319–27. https://doi.org/10.1126/science.187.4174.319.
Zohary D, Hopf M, Weiss E. Domestication of plants in the Old World: the origin and spread of domesticated plants in Southwest Asia, Europe, and the Mediterranean Basin. 4th ed. Oxford: Oxford University Press; 2012.
Zolman BK, Yoder A, Bartel B. Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes. Genetics. 2000;156:1323–37. https://doi.org/10.1093/genetics/156.3.1323.
Zolman BK, Nyberg M, Bartel B. IBR3, a novel peroxisomal acyl-CoA dehydrogenase-like protein required for indole-3-butyric acid response. Plant Mol Biol. 2007;64:59–72. https://doi.org/10.1007/s11103-007-9134-2.
Zolman BK, Martinez N, Millius A, Adham AR, Bartel B. Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes. Genetics. 2008;180:237–51. https://doi.org/10.1534/genetics.108.090399.
Acknowledgements
Not applicable.
Funding
The work in the Cohen laboratory (FPP-S, QT and JDC) is supported by NSF MCB 2225057, USDA National Institute of Food and Agriculture, No. 2019-51181-30025 and 2023-67013-39533, Minnesota Department of Agriculture grant FB#6, University of Minnesota Forever Green Initiative, and by funds from the Minnesota Agricultural Experiment Station and the Gordon and Margaret Bailey Endowment for Environmental Horticulture. The work in the Miller laboratory is supported by the University of Minnesota Agricultural Research, the Education and Extension Tech Transfer program (AGREETT) and the University of Minnesota Arboretum Endowed Land Grant Fund.
Author information
Authors and Affiliations
Contributions
All authors contributed to the review conception and design. The first draft of the manuscript was written by Jerry D. Cohen. Renata P. Pincelli-Souza, Qian Tang, and Brandon M. Miller, who contributed equally to this work, then provided extensive editing. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
Authors declare that they have no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Pincelli-Souza, R.P., Tang, Q., Miller, B.M. et al. Horticultural potential of chemical biology to improve adventitious rooting. HORTIC. ADV. 2, 12 (2024). https://doi.org/10.1007/s44281-024-00034-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s44281-024-00034-7