Abstract
Wheat is a major food crop, with around 765 million tonnes produced globally. The largest wheat producers include the European Union, China, India, Russia, United States, Canada, Pakistan, Australia, Ukraine and Argentina. Cultivation of wheat across such diverse global environments with variation in climate, biotic and abiotic stresses, requires cultivars adapted to a range of growing conditions. One intrinsic way that wheat achieves adaptation is through variation in phenology (seasonal timing of the lifecycle) and related traits (e.g., those affecting plant architecture). It is important to understand the genes that underlie this variation, and how they interact with each other, other traits and the growing environment. This review summarises the current understanding of phenology and developmental traits that adapt wheat to different environments. Examples are provided to illustrate how different combinations of alleles can facilitate breeding of wheat varieties with optimal crop performance for different growing regions or farming systems.
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Introduction
Genes for phenology and plant development, their interactions with each other and the environment largely determine if a wheat (Triticum aestivum L.) crop is successful. For instance, in order to reach maximum seed size and number (potential yield), wheat must establish, develop biomass and flower at a time that coincides with optimal seasonal conditions (Trethowan 2014). Flowering in winter risks frost damage to reproductive structures, and suboptimal radiation levels can reduce yield (Dreccer et al. 2018). Alternatively, if crops flower too late in warm and dry environments, heat damage and water limitation can reduce yield (Flohr et al. 2017). Other aspects of plant biology beyond development are important for adaptation, including winter hardiness and plant architecture, and these must also be co-ordinated with seasonal development.
Understanding the genetic basis for variation in phenology and other adaptive traits can inform crop breeding strategies and contribute to prediction of yield risks, such as drought, frost or heat, and thereby improve crop management. This review focusses on the molecular genetics of wheat adaptation, and how this knowledge can facilitate breeding wheat adapted to diverse growing environments or different farming systems.
Defining and measuring wheat development
Development is the progression of the plant lifecycle, independent of growth that is due to accumulation of biomass. Development comprises distinct phases outlined in Fig. 1. Feekes developed a scale (stages 1–11) classifying the wheat lifecycle from tillering, stem elongation, heading and flowering, through to ripening (Fig. 1b.) Another developmental scale developed by Haun (1973) quantifies progressive leaf emergence on the main stem of wheat, which can then be used to determine leaf emergence rate, otherwise known as phyllochron. In addition, a comprehensive scale describing the wheat lifecycle from germination through to ripening in a two-digit computer-compatible decimal format was developed (Zadoks et al. 1974). The “Zadoks scale” comprises 100 stages describing development of the wheat plant (Fig. 1c).
The wheat seed usually contains four leaf primordia, and more develop on the vegetative meristem during seedling growth (Z10–Z19). Leaf primordia appear as ridges on the apex, before elongation and differentiation into leaves. The position of emerging leaves is predictable with each new leaf develo** on the opposing side of the apex to its predecessor. When around three non-embryonic leaves have developed, tiller buds located in the axils of leaves differentiate to produce tillers (branches) sequentially: tiller 1 from the axil of leaf 1, tiller 2 from leaf 2 and so on. Exceptions to this ordered leaf and tiller development have been described and may be environmentally dependent (Percival 1921). Each tiller has potential to produce secondary tillers. The overall extent of branching, tiller survival and fertility are affected by temperature, light, nutrient status and row spacing. Genetic control of tillering has also been identified (Hyles et al. 2017; Zhao et al. 2019). The primary stem continues to produce tillers, until the plant transitions to the stem elongation (reproductive) phase.
A pivotal point in the wheat lifecycle is transition of the shoot apex from vegetative to reproductive development (Fig. 1a, Waddington et al. 1983). At this stage, production of new leaf primordia ceases, and spikelet formation begins. This represents a commitment to flowering and determines the final leaf number (Wang et al. 1995). The shoot apex elongates, followed by formation of two ridges on the sides of the shoot apex, where previously only single ridges were formed. These can be visualised microscopically; when the plant has reached double-ridge stage, vegetative-to-reproductive transition is complete (Slafer et al. 2015). The lower ridge is a leaf primordium that will later abort, while the upper ridge is the spikelet primordium that will differentiate to form all the floret organs: glume, lemma, palea and stamens of the floret (Moncur 1981). Subsequently, the terminal spikelet forms, and thereafter no further spikelets are formed on the primary axis. The duration of development from double ridge to the terminal spikelet stage is the primary determinant of maximum spikelet number (Rawson 1970).
Simultaneous to early stages of reproductive shoot apex development, stem elongation proceeds. Nodes formed during vegetative development thicken and become a point of rapid growth and extension to form internodes, with each successive internode longer than its predecessor (Evans 1975). This provides a means for the develo** spike to travel upwards through the stem from Z30 onwards. As the stem elongates, spikelet differentiation and floret development also occur. Wheat adjusts its growth in response to environmental stress so that the last-formed spikelets at the base and tip are the first to abort in poor-growing conditions. Usually up to 12 floret primordia are formed in each spikelet; however, only 3–5 survive and set seed, thought to be a function of the competition for resources between spikes and stems during the elongation phase (Kirby 1988).
Synchrony of each developmental phase with optimal seasonal conditions is necessary to optimise production of biomass and yield. For instance, grain number and thus yield in wheat is largely determined by growth rates during the critical period that extends from emergence of the penultimate leaf until early grain filling (Dreccer et al. 2018). Agronomically, it is thus vital to align this sensitive stage to the likely occurrence of seasonal conditions (temperature, radiation and water availability) most conducive to wheat growth. The timing of developmental phases also influences abiotic stress tolerance such as winter hardiness. Seasonal conditions and regional factors, including available moisture, temperature, latitude and day length, all influence the duration of developmental phases (Slafer and Rawson 1994; Angus and Moncur 1977; Amir and Sinclair 1991; Trethowan et al. 2006). This dependence of crop phasic development upon the growing environment represents a strong genotype by environment interaction, and acts to synchronise the lifecycle with external conditions.
Early studies demonstrated that the switch from vegetative to reproductive development is promoted by prolonged cold temperatures of winter (vernalisation) (Chouard 1960). The duration of cold is important, for instance, a plant that responds by flowering after a “cold snap” in autumn would not survive in climates with long, cold winters. From a developmental perspective, vernalisation influences the duration of the vegetative phase, and is a large determinant of the final leaf number. Vernalisation requirement is typically combined with day-length-responsive flowering, such that plants that have vernalised over winter will flower rapidly as days subsequently lengthen in spring (Chouard 1960). This led to the “long-day” and “winter-type”, classification of wheat. That is, the naturally occurring ancestral plant type (wild type) requires vernalisation followed by increasing photoperiod in order to flower. In regions with cold winters, autumn sowing of these types allows flowering to coincide with favourable temperatures and radiation in early summer for optimum yield.
Interaction of plant development and the environment
Alternative life-cycle strategies facilitate adaptation to different environments (Evans et al. 1975). Unlike winter types, spring wheats require little-to-no environmental inducement for flowering (Chouard 1960). These types typically flower rapidly without vernalisation, with rapid progression to the double-ridge stage, and reduced final leaf number relative to winter wheat in similar growing conditions. Spring wheat can also have varying levels of sensitivity to day length. Day-length-insensitive spring cultivars can progress to the terminal spikelet stage and flower rapidly even in short days. Taken together, the absence of vernalisation or day-length requirements allows some spring wheats to be sown in environments with milder winters and at different times of the year (see “Quantitative traits in the farming system”, Fig. 3). From a study of wild emmer wheat Triticum dicoccoides, it is thought that spring types evolved from wild-type winter habit in the progenitor of cultivated hexaploid wheat (Kato et al. 1997).
Since wheat can be grown across diverse environments and at different times of the year, it is useful to calibrate development versus temperature and day length using accumulated thermal time or degree-days (DD), or photo-degree days (PDD). This allows comparison of developmental rates across different conditions, where the rate of development per se differs. For DD (Eq. 1), calculations are based on accumulated temperature above a base, and may also consider an upper limit so that only temperatures conducive to plant development are considered. DD can be determined by summing daily average temperatures as the equation below, or considers more frequent measures of temperature or estimates thereof, for example, using sine curve or triangular equations (McMaster and Wilhelm 1997; Zalom et al. 1983; Snyder 1985).
Equation 1. Estimation of thermal time
DD(ave) = Degree-days, average calculation (°C d)
Tmax = Maximum daily temperature (°C)
Tmin = Minimum daily temperature (°C)
Tbase = Base temperature, typically 0 °C or 5 °C, dependent on growth stage
In a study by Bloomfield et al. (2018), development of near-isogenic lines (NILs) was recorded (in DD) under inductive growth conditions; the approximate cumulative DDs to heading and flowering relative to other scales of development are shown in Fig. 1d (Bloomfield, pers. comm.). Comparison of slow-develo** wheats (photoperiod-sensitive winter types) versus fast-develo** wheats (photoperiod-insensitive spring types) illustrates the variation in response to temperature between these different classes.
To determine PDD, cumulative time from sunrise to civil twilight (day length) can be incorporated through the following equation (Wilsie 1962):
Equation 2. Estimation of photo-thermal time
PDD = Photo-degree days (°C d h)
DD = Degree-days (°C d)
t = day-length (h)
A similar approach can be applied to calibrate temperature accumulation during vernalisation. Vernal days, the cumulative time in days until vernalisation saturation is reached (i.e., double-ridge stage reached), are determined by summing days from germination to development of the final leaf (Robertson et al. 1996). Porter and Gawith (1999) suggest that vernalisation occurs most rapidly at 4.9 °C, and requires temperatures between −1.3 and 15.7 °C.
Molecular pathways of wheat development
Since the phenology of wheat determines adaptation to different environments, an understanding of the genes underlying developmental variation is paramount. The major genes affecting wheat phenology (see Fig. 2) are those related to vernalisation requirement, photoperiod sensitivity and earliness per se, which is the duration of development until flowering, in conditions where vernalisation and photoperiod requirements are met.
Vernalisation pathway
The key component of vernalisation requirement of wheat is the VERNALIZATION1 (VRN1) locus, with a copy on the long arm of chromosome 5, in each of the A, B and D sub-genomes. VRN1 encodes an MIKC-type MADS box (MINICHROMOSOME MAINTENANCE1/AGAMOUS/DEFICIENS/SERUM RESPONSE FACTOR), with a conserved 60 amino-acid MADS box DNA- binding domain and three additional domains I (intervening), K (keratin-like) and a C-terminal domain. VRN1 is most like the APETALA1/FRUITFULL class (AP1/FUL) of MADS box genes of Arabidopsis thaliana. These genes play important roles in floral development in Arabidopsis, and can trigger early flowering when expressed at high levels (Mandel and Yanofsky 1995). Unlike the AP1/FUL genes of Arabidopsis, transcription of VRN1 increases with exposure to prolonged cold (Danyluk et al. 2003; Trevaskis et al. 2003; Yan et al. 2003). It seems that VRN1 evolved from recruitment of the floral-promoting potential of AP1/FUL genes to provide a low-temperature-induced flowering switch. This role for AP1/FUL-like genes is seemingly unique to the temperate grasses. VRN1 is expressed in both leaves and shoot apices of vernalised plants; accumulation of VRN1 transcripts in the shoot apex is associated with the switch to reproductive development, while transcription of VRN1 in leaves facilitates the long-day flowering response after winter (Fig. 2).
The precise mechanism that mediates low-temperature induction of VRN1 is not known, but histone modifications appear to play a role. Epigenetic modification of chromatin by histone modification or methylation of DNA has been well studied and linked to heritable changes in gene expression and phenotypic variance (see Banta and Richards (2018) for review). Histone modifications mediate downregulation of the Arabidopsis flowering repressor FLOWERING LOCUS C during vernalisation (Finnegan et al. 2005). In cereals, before vernalisation, histones at the promoter and the first intron of the VRN1 locus have modifications associated with gene repression (histone 3 lysine 27 trimethylation, H3K27me3), and during vernalisation, there is a shift towards modifications typical of active genes (histone 3 lysine 4 trimethylation, H3K4me3) (Oliver et al. 2009). These histone modifications potentially maintain repression of VRN1 before winter and conversely, sustain activity of VRN1 after prolonged cold. This could provide a “memory” of vernalisation, such that chromatin at the VRN1 locus remains in an active state after winter even when temperatures rise, allowing flowering to proceed when days lengthen in spring (Oliver et al. 2009). Presumably, the chromatin state is restored during meiosis, as the vernalisation requirement “resets” in progeny. During seed development, cold conditions while ripening can vernalise the progeny seed, and this memory of vernalisation is retained post seed development, drying and harvest (Gregory and Purvis 1936; Atayde 2019). The implications of this need to be considered during seed increases and crop** situations.
Mutations in the promoter and deletions in the large first intron of VRN1 are both associated with elevated expression of the gene in the absence of cold and accelerated flowering without vernalisation (Kippes et al. 2018). These mutations are found in the VRN1 gene from each of the A, B and D genomes, and give rise to dominant alleles for reduced vernalisation requirement, with the A-genome version conferring the greatest effect (no requirement for cold temperature to flower) relative to the B- and D-genome alleles (reduced vernalisation requirement, semi-spring types) (Trevaskis et al. 2003). The difference between the sub-genomes is potentially due to the nature of the mutations found in each allele (i.e., promoter insertion plus gene duplication on A genome, intron deletions of differing size on B and D genomes).
The first intron of VRN1 contains a binding site for the T. aestivum glycine-rich RNA-binding protein 2 (TaGRP2), which blocks expression of VRN1 until it is released by cold. During sustained low temperatures, TaGRP2 interacts with a jacalin lectin carbohydrate-binding protein TaVER2 (vernalisation-related 2) via O-GlcNAc (O-linked β-N-acetyl glucosamine) (** and epistatic interactions of the vernalization gene VRN-D4 in hexaploid wheat. Mol Genet Genomics 289:47–62" href="/article/10.1038/s41437-020-0320-1#ref-CR57" id="ref-link-section-d255753035e1108">2014). VRN4 is associated with increased VRN1 transcript levels from the extra gene copy at the VRN4 locus, and thus reduced vernalisation requirement. The copy of VRN1 at the VRN4 locus contains the intron SNPs described earlier (those which disrupt TaGRP2 binding in VRN1), which potentially explains why VRN1 transcription is elevated in wheats that carry VRN4. The origin of VRN4 in Australian cultivars has been traced to cv. Gabo (Kippes et al. 2015), an important cultivar introducing spring-growth habit and adaptation to the Australian climate.
Other MADS box genes also play roles in regulation of wheat flowering. Two other AP1/FUL-like genes TaFUL2 and TaFUL3 are paralogues of VRN1 that regulate spike development and also influence flowering time, though to a lesser extent than VRN1 (Li et al. 2019). Another MADS box gene, ODDSOC2 (OS2) (also known as TaAGL33 and TaAGL22 in wheat) is a repressor of flowering downregulated by vernalisation (Greenup et al. 2010, 2011). A Short vegetative phase-like gene, Vegetative to reproductive transition 2 (VRT2), located on the short arm of group 7 chromosomes, was suggested to be a repressor of floral development downregulated by cold (Kane et al. 2005), but subsequent studies found that transcription of this gene increases at low temperatures, and that VRT2 more likely activates flowering in cooperation with VRN1 (Trevaskis et al. 2007; ** of the earliness per se-3A (Eps-3A) locus in diploid einkorn wheat and its relation to the syntenic regions in rice and Brachypodium distachyon L. Mol Breed 30:1097–1108" href="/article/10.1038/s41437-020-0320-1#ref-CR37" id="ref-link-section-d255753035e1798">2012). Another EPS locus, Eps-Am1, encompasses a deletion of the wheat ELF3 gene (Zikhali et al. 2016). Ochagavía et al. (2019) reports that allelic differences at TaELF3 confer differing levels of sensitivity to temperature; earliness was associated with an increased sensitivity to temperature during the late reproductive phase of development in hexaploid wheat. The same study also revealed temperature-dependent suppression of TaGI due to TaELF3. Both genes have also been associated with phytochrome-mediated light signalling and the circadian clock (Ford et al. 2016).
Secondary adaptive traits
Adapted wheat contains allelic combinations of the multiple genes affecting phenology to ensure that the lifecycle is appropriate to the growing conditions. Secondary to this, other traits are also important and must be matched to phenology and the environment.
Winter hardiness
In cold climates where wheat is sown in autumn, cultivars require a degree of “winter hardiness” to survive freezing temperatures during the vegetative phase. Key to this is the ability to acclimate to cold, whereby freezing tolerance is acquired in response to low temperatures. This can occur in conjunction with the vernalisation response.
Cold acclimation is mediated by C-repeat-binding factors (CBF), also known as dehydration-responsive element binding (DREB) proteins. CBF/DREBs contain a DNA motif of approximately 60 amino acids that bind specific promoter elements (CRT-DRE boxes) of target genes leading to their activation, for instance, late embryogenesis abundant (LEA) (also known as dehydrins (DHNS)) and cold-regulated (COR) genes. Li and Chen (1997) found higher accumulation of DHNS transcripts in winter cereals subject to cold relative to spring types, given the same cold acclimation treatment. Upregulation of a cereal-specific COR gene (wlt10) has been reported in response to low temperature, with accumulation of transcripts more rapid and sustained in a cold-tolerant winter background (Ohno et al. 2001). Soon after exposure to cold, inducer of cbf expression 1 (ICE1) is upregulated, followed by expression of COR genes some hours later. In Arabidopsis, freezing tolerance is related to the subsequent production of cryoprotectants, such as sucrose, raffinose and hydrophilic peptides, which protect membranes against dehydration during freezing (Thomashow 2010). In wheat, changes in the leaf content of lipids, sugars, sugar alcohols and amino acids have been associated with cold acclimation and metabolomics suggested as a measurement tool for chilling and frost tolerance (Cheong et al. 2019).
Not only have CBFs been identified as key components of the cold acclimation pathway, they have also been found to contribute to allelic variation. At least 15 CBFs have been identified in wheat with an important locus, FR2 comprising a cluster of CBF genes close to VRN1 on group 5 chromosomes. Copy-number variation of CBF genes at FRA2 was attributed to increased winter hardiness and therefore adaptation in European winter wheat (Wu̎rschum et al. 2016), while variation at the FRB2 locus was associated with frost tolerance, flowering time and improved yield (Pearce et al. 2013; Badawi et al. 2007; Eagles et al. 2016). The wild-type allele of FRB2 is often present in winter wheat, and is considered advantageous for adaptation and yield in frost-prone environments, opposed to a large deleted segment frequently found in spring types, which should be beneficial in areas with low-frost risk (Eagles et al. 2016, 2018). Genetic linkage of the VRN1 and FR2 loci, and the association of vernalisation sensitivity with particular alleles of FRB2, suggests that co-selection of these independent loci is important for adaptation.
There are broader functions for CBF genes, including regulation of growth and development. These transcription factors are members of the APETALA 2/ethylene-responsive element binding gene family also involved in floral organ identity and drought and salinity stress response (Yamaguchi-Shinozaki and Shinozaki 2006). A controlled condition experiment involving transgenic barley overexpressing TaDREB2 and TaDREB3, showed that plants that constitutively expressed the transgenes grew more slowly, flowered 2–3 weeks later and had changed activity of other CBFs and improved frost tolerance (Morran et al. 2011).
The cold acclimation pathway also potentially plays a role in regulating plant architecture. A feature of many winter-type wheats with a high degree of winter hardiness is early prostrate growth habit, where plants have large tiller angles at the vegetative stage of development (Li and Chen 1997). Prostrate plant types in the vegetative stage might confer adaptation to cold and frosty winters by allowing the plant to be covered by a blanket of snow that protects the crop against freezing temperatures.
Tillering
Aside from prostrate growth habit, another feature of winter wheat is a high degree of tillering, due to the increased duration of the vegetative phase (a vernalisation-requiring wheat will take longer to switch to reproductive development relative to a vernalisation-insensitive plant). A larger number of tillers can increase yield in a high-input (water, nutrient) system due to production of additional fertile spikes. In water-limiting environments however, a higher tiller number may not contribute to increased yield, with additional tillers unable to support fertile spikes. A tiller-reducing gene in wheat, TIN, has been identified and studied for yield effects in water-limiting environments of Australia (Richards 1988). To date, there are conflicting reports of the benefit or disadvantage of reduced tillering due to TIN in Australian farming systems, and it is likely that the limited number of backgrounds in which the gene has been studied, along with a strong genotype × environment interaction is confounding (Mitchell et al. 2012; Hendriks et al. 2016; Fletcher et al. 2019). Exploring the optimal tillering potential in different phenological types would be interesting.
Plant height
Final plant height is another developmental trait that influences adaptation. In high-input irrigated farming systems, cultivars with short stature are required to prevent lodging (Sanchez-Garcia and Bentley 2019), whereas taller cultivars are often suited to low-input dryland systems such as the Australian wheat belt (Mathews et al. 2006). A major determinant of the final plant height is the endogenous supply and sensitivity to the hormone gibberellic acid (GA), which is involved in most aspects of development, including germination, vegetative growth, stem elongation and production of flowers and seeds (see Yamaguchi 2008). GA is also implicated in stress response pathways, for example, drought and salinity (Llanes et al. 2016). Other research shows that GA is an important component of the flowering pathway of grasses (MacMillan et al. 2005) and in barley, early flowering triggered by mutations in HvELF3 requires elevated GA biosynthesis (Boden et al. 2014).
GA promotes growth by an interaction with, and removal of the effect of growth-inhibitory DELLA proteins. In this process, bioactive GA binds to a receptor protein GA-insensitive dwarf 1 (GID1) and DELLA to form a complex that is targeted by an E3 ubiquitin ligase, degrading DELLA (see Sun (2010) for review).
REDUCED HEIGHT 1 (Rht-B1, RHT1, chromosome 4BS) and REDUCED HEIGHT 2 (Rht-D1, RHT2, chromosome 4DS) are homoeologous copies of the same DELLA-encoding gene on the B and D genomes. Mutations in these genes give rise to alleles conferring semi-dwarf habit (reduced stem elongation). These mutations create premature stop codons with subsequent truncated proteins unable to form the GA–GID–DELLA complex. Instead of being degraded, DELLA then accumulates and represses growth. Dwarf alleles Rht-B1b and Rht-D1b have been deployed in plant breeding to develop wheat adapted to environments with high-yield potential. Otherwise known as green revolution genes, they facilitate use of irrigation and nitrogen fertiliser to boost biomass production, harvest index and yield, by ensuring that crops are adapted to high-input farming systems and do not lodge (Peng et al. 1999). Dwarf alleles can be traced to a Japanese landrace, which was introgressed with US germplasm to create the cultivar Norin-10. This germplasm was then deployed by Norman Borlaug in the International Maize and Wheat Improvement Centre (CIMMYT) breeding program. Alleles from Norin-10 then spread to breeding programs throughout the world via cultivars Pitic 62, Penjamo 62 and their progeny. The success of these cultivars is due to their reduced height and also likely improvement in productive tiller number to increase yield (Evans 1975). Other dwarf alleles of Rht-B1 and Rht-D1 have been identified at these loci conferring differing levels of height reduction that may be useful for adaptation in different environments (Pearce et al. 2011).
An international trial found that in high-yielding environments, on average, there is no yield penalty associated with Rht-B1b and Rht-D1b relative to wild-type alleles in near-isogenic tall lines (Mathews et al. 2006). In low-yielding sites however, semi-dwarfs yielded less than the tall wild-type NIL, and so breeding for taller semi-dwarfs, or “short-talls” would be ideal for adaptation and yield in these environments. This result may reflect the disadvantage of dwarf alleles of Rht-B1 and Rht-D1 loci, that the whole plant is insensitive to GA. This means that after germination, the growing sheath that delivers the shoot from the seed to soil surface (coleoptile) is also reduced in length. For this reason, Rht-B1b- and Rht-D1b-carrying lines cannot be sown as deep as their wild-type counterparts. This can have a negative impact on establishment and the ability to capture soil moisture deep in the profile (Whan 1976).
Other dwarfing genes responsive to GA and so with potential to maintain long coleoptiles have been described in wheat (Ellis et al. 2004). Recently, a mutant with lower endogenous GA content (originally described in durum) was identified as Rht18 on chromosome 6AS (Ford et al. 2018). An agronomic study (Tang 2016) suggests that Rht18 is a promising candidate to replace Rht-D1b. Haque et al. (2011) proposed that Rht14 and Rht16 are alleles at the same locus, and based on the map location of Rht24 in Chinese Spring (Wu̎rschum et al. 2017), it is possible that this gene is allelic to Rht18. A distinct locus on chromosome 6A, Rht25, reduced height to a lesser extent than Rht-B1b and Rht-D1b (Mo et al. 2018), and may be a good candidate to produce “short-talls”. Other dwarfing genes, including Rht4, Rht5 and Rht8, are attractive breeding targets for adaptation if they are not associated with growth penalties such as short coleoptiles (Ellis et al. 2004).
There is a coincidence of height and phenology, and studies have detected an association of VRN1 and PPD1 with plant height in both diverse and structured genetic wheat populations (Camargo et al. 2018; Wilhelm et al. 2013). It is important to consider dwarfing genes and phenological variation together as gene–gene and gene–environment interactions will affect the final plant height.
Quantitative traits in the farming system
Phenology is fundamental to the adaptation of wheat. This is particularly evident in the crop** regions of Australia. Cultivars with a strong vernalisation requirement and sensitivity to day length are suited to regions of Australia which have cold winters and a high risk of frost (Fig. 3). Most of the wheat-growing regions of Australia have milder winters and hot and dry summers, so wheats with a shorter lifecycle from lack of vernalisation requirement and day-length sensitivity (spring types) are traditionally sown after late autumn rain and flower early in spring, before temperature and drought stress in summer (Fig. 3). In response to a changing climate, a field and simulation study assessed performance of different combinations of development alleles in near-isogenic lines (Hunt et al. 2019), and suggested that a shift to earlier sowing of slower-develo** genotypes in these regions would increase yield, despite the predicted decrease in rainfall and increase in temperature. For this to occur, Australian breeders need to develop cultivars with slower rates of development and flowering behaviour matched to each growing environment. This is possible with the use of high-throughput marker platforms in breeding programmes to select allelic combinations for adaptation (Grogan et al. 2016). Other traits, such as plant architecture and tolerance to climatic stress, are also important to optimise yield in each farming system. The complex network of genes that underlie adaptation interact strongly with the environment, and in a changing climate, breeding new cultivars and changing agronomic practices will be required to ensure future crop success.
Future possibilities
The current understanding of phenology and adaptation was developed through reductionist approaches, such as gene map** in biparental populations, and detailed studies of NILs, to determine the genetic basis and develop molecular markers for individual traits. These approaches are often time consuming and labour intensive. Emerging technologies, including whole-genome sequencing, high-throughput genoty** and genome-wide analytical techniques, are accelerating progress and allow research to be conducted at a larger, more holistic scale. The transcriptome for instance, captures the response of the genome to the environment. Transcriptome analysis of diverse genetic material adapted to different climates around the globe should provide new insights. Other data, such as proteomics and metabolomics, will also be invaluable, and analytical techniques such as machine learning, utilised to handle different types of data at scale. Technologies that allow rapid resolution of complex systems will be important to harness quantitative traits for future crop improvement, particularly where these traits exhibit strong environmental interactions.
Conclusion
Quantitative traits are complex due to the action of multiple genes and their interactions with each other and the environment, giving rise to a continuous distribution of phenotypes. Phenology and plant architecture are examples of quantitative traits that are fundamental contributors to the adaptation of wheat. Major loci include VRN, PPD, EPS, RHT and genes from the CBF/DREB family, though there are many other minor-affect loci that are important for adaptation. It is a worthy pursuit to characterise the genes that underlie these traits, and most relevant if the effect of alleles can be assessed in the growing environment that best reflects the farmer’s field. In this way, breeders can target allelic combinations for specific wheat-growing regions and farm management systems. As the global climate changes, new allelic combinations may be required for the adaptation of wheat. For breeders to deliver future adapted cultivars, expedited methods of research to understand gene pathways in relevant environments alongside development of markers for selection are required.
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Acknowledgements
This review was undertaken during Jessica Hyles’ PhD. We are grateful to Dr Howard Eagles for his mentorship and the University of Sydney for financial support. The authors thank the reviewers for their thoughtful critique.
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Hyles, J., Bloomfield, M.T., Hunt, J.R. et al. Phenology and related traits for wheat adaptation. Heredity 125, 417–430 (2020). https://doi.org/10.1038/s41437-020-0320-1
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DOI: https://doi.org/10.1038/s41437-020-0320-1
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