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GhLIP1, a lipoic acid synthase gene, negatively regulates leaf senescence in cotton

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Abstract

Leaves are the key organs of plants that produce photosynthates. Leaf senescence aids nutrient remobilization from source to sink tissues, which dramatically affects crop quality and yield. Although several senescence-associated genes (SAGs) have been recognized in cotton, the function of lipoic acid synthase in leaf senescence remains unclear. Therefore, we isolated a lipoic acid synthase gene named GhLIP1 from cotton (Gossypium hirsutum L.). Protein domain analysis revealed that GhLIP1 had a LIAS-N domain and an Elp3 domain, and yeast mutant complementation experiments demonstrated that GhLIP1 was a lipoic acid synthase. GhLIP1 expression pattern analysis showed that GhLIP1 was vastly expressed in fibres, and the phytohormone IAA (indole-3-acetic acid) induced its transcription. When GhLIP1 was transformed into Arabidopsis, the leaves of overexpression Arabidopsis exhibited a late leaf senescence phenotype compared to wild-type Arabidopsis, Col-0. Moreover, downregulation of GhLIP1 expression using virus-induced gene silencing (VIGS) technology resulted in early leaf senescence in cotton. qRT-PCR analyses revealed that two SAGs, GhWRKY53 and GhNAP, were upregulated in cotton plants with GhLIP1 knock-down. Cell ultrastructure observations found that chloroplasts were degraded in an orderly manner in cotton leaf cells with GhLIP1 knock-down. These results suggest that GhLIP1 plays a significant role in leaf senescence in cotton.

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References

  • Babiychuk E, Vandepoele K, Wissing J, Garcia-Diaz M, De Rycke R, Akbari H, Joubes J, Beeckman T, Jansch L, Frentzen M, Van Montagu MCE, Kushnir S (2011) Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proc Natl Acad Sci USA 108:6674–6679

    Article  CAS  PubMed  Google Scholar 

  • Balazadeh S, Siddiqui H, Ad A, Lp MR, Caldana C, Mehrnia M, Mi Z, Khler B, Muellerroeber B (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62:250–264

    Article  CAS  PubMed  Google Scholar 

  • Balazadeh S, Schildhauer J, Araújo WL, Munné-Bosch S, Fernie AR, Proost S, Humbeck K, Mueller-Roeber B (2014) Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences. J Exp Bot 65:3975–3992

    Article  PubMed  PubMed Central  Google Scholar 

  • Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol 134:1784–1792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang CJ, Morris K, Jenner C, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, Denby K, Mead A, Buchanan-Wollaston V (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brouwer B, Ziolkowska A, Bagard M, Keech O, Gardestrom P (2012) The impact of light intensity on shade-induced leaf senescence. Plant Cell Environ 35:1084–1098

    Article  PubMed  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  CAS  PubMed  Google Scholar 

  • Chen ER, Wang XQ, Gong Q, Butt HI, Chen YL, Zhang CJ, Yang ZR, Wu ZX, Ge XY, Zhang XL, Li FG, Zhang XY (2017) A novel GhBEE1-Like gene of cotton causes anther indehiscence in transgenic Arabidopsis under uncontrolled transcription level. Gene 627:49–56

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara K, Okamura-Ikeda K, Motokawa Y (1990) cDNA sequence, in vitro synthesis, and intramitochondrial lipoylation of H-protein of the glycine cleavage system. J Biol Chem 265:17463–17467

    Article  CAS  PubMed  Google Scholar 

  • Gan S, Amasino RM (1997) Making sense of senescence (Molecular genetic regulation and manipulation of leaf senescence). Plant Physiol 113:313–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MFO, Yariv I, Dor C, Bassani M (2004) Large-scale identification of leaf senescence-associated genes. Plant J 36:629–642

    Article  Google Scholar 

  • Guinn G (1985) Abscisic acid and cutout in cotton. Plant Physiol 77:16–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo P, Li Z, Huang P, Li B, Fang S, Chu J, Guo H (2017) A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence. Plant Cell 29:2854–2870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang G, Wu Z, Percy RG, Bai M, Li Y, Frelichowski JE, Hu J, Wang K, Yu JZ, Zhu Y (2020) Genome sequence of Gossypium herbaceum and genome updates of Gossypium arboreum and Gossypium hirsutum provide insights into cotton A-genome evolution. Nat Genet 52:516–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang YJ, Liang G, Yang SZ, Yu DQ (2014) Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell 26:230–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jibran R, Hunter DA, Dijkwel PP (2013) Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol Biol 82:547–561

    Article  CAS  PubMed  Google Scholar 

  • **g HC, Schippers JH, Hille J, Dijkwel PP (2005) Ethylene-induced leaf senescence depends on age-related changes and OLD genes in Arabidopsis. J Exp Bot 56:2915–2923

    Article  CAS  PubMed  Google Scholar 

  • Kim Y, Oliver DJ (1990) Molecular cloning, transcriptional characterization, and sequencing of cDNA encoding the H-protein of the mitochondrial glycine decarboxylase complex in peas. J Biol Chem 265:848–853

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci USA 103:814–819

    Article  CAS  PubMed  Google Scholar 

  • Kusaba M, Tanaka A, Tanaka R (2013) Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence. Photosynth Res 117:221–234

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Seo PJ, Lee HJ, Park CM (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70:831–844

    Article  CAS  PubMed  Google Scholar 

  • Leopold AC (1961) Senescence in plant development: the death of plants or plant parts may be of positive ecological or physiological value. Science 134:1727–1732

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Peng J, Wen X, Guo H (2012) Gene network analysis and functional studies of senescence-associated genes reveal novel regulators of Arabidopsis leaf senescence. J Integr Plant Biol 54:526–539

    Article  CAS  PubMed  Google Scholar 

  • Liang CZ, Wang YQ, Zhu YN, Tang JY, Hu B, Liu LC, Ou SJ, Wu HK, Sun XH, Chu JF, Chu CC (2014) OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc Natl Acad Sci USA 111:10013–10018

    Article  CAS  PubMed  Google Scholar 

  • Lim PO, Woo HR, Nam HG (2003) Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Sci 8:272–278

    Article  CAS  PubMed  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  PubMed  Google Scholar 

  • Lin M, Pang CY, Fan SL, Song MZ, Wei HL, Yu SX (2015) Global analysis of the Gossypium hirsutum L. transcriptome during leaf senescence by RNA-SEq. BMC Plant Biol 15:43

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu J, Pang CY, Wei HL, Song MZ, Meng YY, Ma JH, Fan SL, Yu SX (2015) iTRAQ-facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild-type cotton (Gossypium hirsutum L.). J Proteomics 126:68–81

    Article  CAS  PubMed  Google Scholar 

  • Macherel D, Lebrun M, Gagnon J, Neuburger M, Douce R (1990) cDNA cloning, primary structure and gene expression for H-protein, a component of the glycine-cleavage system (glycine decarboxylase) of pea (Pisum sativum) leaf mitochondria. Biochem J 268:783–789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattevi A, de Kok A, Perham RN (1992) The pyruvate dehydrogenase multienzyme complex. Curr Opin Struc Biol 2:877–887

    Article  CAS  Google Scholar 

  • Miller JR, Busby RW, Jordan SW, Cheek J, Henshaw TF, Ashley GW, Broderick JB, Cronan JE, Marletta MA (2000) Escherichia coli LipA is a lipoyl synthase: In vitro biosynthesis of lipoylated pyruvate dehydrogenase complex from octanoyl-acyl carrier protein. Biochemistry 39:15166–15178

    Article  CAS  PubMed  Google Scholar 

  • Nam HG (1997) The molecular genetic analysis of leaf senescence. Curr Opin Biotechnol 8:200–207

    Article  CAS  PubMed  Google Scholar 

  • Noodén LD (1988) The Phenomena of Senescence and Aging. In: Noodén LD, Leopold AC (eds) Senescence and Aging in Plants. Academic Press, pp 1–50

  • Oh SA, Sang YL, Chung IK, Lee CH, Hong GN (1996) A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol Biol 30:739–754

    Article  CAS  PubMed  Google Scholar 

  • Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pang J, Zhu Y, Li Q, Liu J, Tian Y, Liu Y, Wu J (2013) Development of Agrobacterium-mediated virus-induced gene silencing and performance evaluation of four marker genes in Gossypium barbadense. PLoS One 8:e73211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perham RN (1991) Domains, motifs, and linkers in 2-oxo acid dehydrogenase multienzyme complexes: a paradigm in the design of a multifunctional protein. Biochemistry 30:8501–8512

    Article  CAS  PubMed  Google Scholar 

  • Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282

    Article  CAS  PubMed  Google Scholar 

  • Reed KE, Cronan JE Jr (1993) Lipoic acid metabolism in Escherichia coli: sequencing and functional characterization of the lipA and lipB genes. J Bacteriol 175:1325–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed LJ, Hackert ML (1990) Structure-function relationships in dihydrolipoamide acyltransferases. J Bio Chem 16:8971–8974

    Article  Google Scholar 

  • Ren MZ, Venglat P, Qiu SQ, Feng L, Cao YG, Wang E, **ang DQ, Wang JH, Alexander D, Chalivendra S, Logan D, Mattoo A, Selvaraj G, Datla R (2012) Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. Plant Cell 24:4850–4874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richard-Molard C, Krapp A, Brun F, Ney B, Daniel-Vedele F, Chaillou S (2008) Plant response to nitrate starvation is determined by N storage capacity matched by nitrate uptake capacity in two Arabidopsis genotypes. J Exp Bot 59:779–791

    Article  CAS  PubMed  Google Scholar 

  • Rouse D, Mackay P, Stirnberg P, Estelle M, Leyser O (1998) Changes in auxin response from mutations in an AUX/IAA gene. Science 279:1371–1373

    Article  CAS  PubMed  Google Scholar 

  • Senchina DS, Alvarez I, Cronn RC, Liu B, Rong JK, Noyes RD, Paterson AH, Wing RA, Wilkins TA, Wendel JF (2003) Rate variation among nuclear genes and the age of polyploidy in Gossypium. Mol Biol Evol 20:633–643

    Article  CAS  PubMed  Google Scholar 

  • Shi HT, Chen L, Ye TT, Liu XD, Ding KJ, Chan ZL (2014) Modulation of auxin content in Arabidopsis confers improved drought stress resistance. Plant Physiol Bioch 82:209–217

    Article  CAS  Google Scholar 

  • Shoji K, Addicott FT, Swets WA (1951) Auxin in relation to leaf blade abscission. Plant Physiol 26:189–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh VP, Jegadheesan A (2003) Effect of alpha-lipoic acid on senescence in gladiolus flowers. Indian J Plant Physiol Special Issue No 1:72–79

    Google Scholar 

  • Sulo P, Martin NC (1993) Isolation and characterization of LIP5. A lipoate biosynthetic locus of Saccharomyces cerevisiae. J Biol Chem 268:17634–17639

    Article  CAS  PubMed  Google Scholar 

  • van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge UI, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, Chen E, Ge X, Gong Q, Butt H, Zhang C, Yang Z, Li F, Zhang X (2018) Overexpressed BRH1, a RING finger gene, alters rosette leaf shape in Arabidopsis thaliana. Sci China Life Sci 61:79–87

    Article  CAS  PubMed  Google Scholar 

  • Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469

    Article  CAS  PubMed  Google Scholar 

  • Webber JM (1936) Cytogenetic notes on cotton and cotton relatives. II Science 84:378

    CAS  PubMed  Google Scholar 

  • Wendel JF (1989) New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci USA 86:4132–4136

    Article  CAS  PubMed  Google Scholar 

  • Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-Box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13:1779–1790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woo HR, Koo HJ, Kim J, Jeong H, Yang JO, Lee IH, Jun JH, Choi SH, Park SJ, Kang B, Kim YW, Phee BK, Kim JH, Seo C, Park C, Kim SC, Park S, Lee B, Lee S, Hwang D, Nam HG, Lim PO (2016) Programming of plant leaf senescence with temporal and inter-organellar coordination of transcriptome in Arabidopsis. Plant Physiol 171:452–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright BP (1998) Research into early senescence syndrome in cotton. Better Crops International 12:14–16

    Google Scholar 

  • Yang SD, Seo PJ, Yoon HK, Park CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuno R, Wada H (1998) Biosynthesis of lipoic acid in Arabidopsis: cloning and characterization of the cDNA for lipoic acid synthase. Plant Physiol 118:935–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuno R, Wada H (2002) The biosynthetic pathway for lipoic acid is present in plastids and mitochondria in Arabidopsis thaliana. Febs Lett 517:110–114

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Jiang T, Liu Z, Zhang W, Jian G, Qi F (2012) Dominant gene cplsr1 corresponding to premature leaf senescence resistance in cotton (Gossypium hirsutum L.). J Integr Plant Biol 54:577–583

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Wang J, Cheng Y, Chi YJ, Fan B, Yu JQ, Chen Z, Gassmann W (2013) NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PloS Genet 10:e1004477

    Google Scholar 

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Acknowledgements

We thank Dr. Shijun Chen of the Experimental Center at Henan Institute of Science and Technology for his help with the cell ultrastructure observations.

Funding

This work was supported by the National Natural Science Foundation of China (Grant Number 31872129) and Henan Science and Technology Project (Grant Number 202102110146).

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Contributions

EY Chen and CW Li conceived and designed the research; EY Chen, HY Hu, XB Yang, DX Li and QC Wei performed the experiments; F Zhou, YY Guan, YA Yu and PW Song analyzed the data; EY Chen and CW Li wrote, reviewed and edited the manuscript. All authors read and approved the final manuscript.

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Correspondence to Chengwei Li.

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The authors declare that they have no conflicts of interest.

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Communicated by Longbiao Guo.

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Fig. S1

Multiple sequence alignment of the GhLIP1 protein and its homologs in other species. (PDF 16 kb)

Fig. S2

Phenotypes of cotton plants with down-regulated expression of GhLIP1 and GhPDS using VIGS technology. The TRV2::GhPDS cotton line was used as a positive control in the VIGS procedure. (TIF 7179 kb)

Table S1

Primers used in this study. Table S2 The qRT-PCR primers specifically used for the analysis of GhLIP1 and senescence-associated gene expression patterns. (DOCX 15 kb)

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Chen, E., Hu, H., Yang, X. et al. GhLIP1, a lipoic acid synthase gene, negatively regulates leaf senescence in cotton. Plant Growth Regul 94, 73–85 (2021). https://doi.org/10.1007/s10725-021-00697-6

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