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Metabolic characteristics of self-pollinated wheat seed under red and blue light during early development

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Abstract

Main conclusion

Blue light has a greater effect on jasmonic acid and flavonoid accumulation in wheat seeds than red light; blue light reduces starch synthesis and the size of starch granules and seeds.

Abstract

This study sought to elucidate the effects of blue and red light on seed metabolism to provide important insights regarding the role of light quality in regulating seed growth and development. We used combined multi-omics analysis to investigate the impact of red and blue light (BL) on the induction of secondary metabolite accumulation in the hexaploid wheat Dianmai 3 after pollination. Flavonoids and alkaloids were the most differentially abundant metabolites detected under different treatments. Additionally, we used multi-omics and weighted correlation network analysis to screen multiple candidate genes associated with jasmonic acid (JA) and flavonoids. Expression regulatory networks were constructed based on RNA-sequencing data and their potential binding sites. The results revealed that BL had a greater effect on JA and flavonoid accumulation in wheat seeds than red light. Furthermore, BL reduced starch synthesis and stunted the size of starch granules and seeds. Collectively, these findings clarify the role of BL in the metabolic regulation of early seed development in wheat.

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Data availability statement

The original contributions presented in the study are publicly available. This data can be found here National Center for BiotechnologyInformation (NCBI) SRA database under accession number PRJNA953095.

Abbreviations

BA:

Black bag

BL:

Blue light

BU:

Blue bag

CK:

Control plants

DEG:

Differentially expressed gene

DAMs:

Differentially accumulated metabolites

DAP:

Days after pollination

JA:

Jasmonic acid

RD:

Red bag

TR:

Colorless bag

WCGNA:

Weighted correlation network analysis

References

  • Bailey T, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36

    CAS  PubMed  Google Scholar 

  • Ballare CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65:335–363

    Article  CAS  PubMed  Google Scholar 

  • Barnes C, Bugbee B (1992) Morphological responses of wheat to blue light. J Plant Physiol 139:339–342

    Article  CAS  PubMed  Google Scholar 

  • Barrero JM, Downie AB, Xu Q, Gubler F (2014) A role for barley cryptochrome1 in light regulation of grain dormancy and germination. Plant Cell 26:1094–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartucca ML, Guiducci M, Falcinelli B, Del Buono D, Benincasa P (2020) Blue: red LED light proportion affects vegetative parameters, pigment content, and oxidative status of einkorn (Triticum monococcum L. ssp. monococcum) wheat grass. J Agric Food Chem 68:8757–8763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhoite R, Si P, Siddique KHM, Yan G (2021) Comparative transcriptome analyses for metribuzin tolerance provide insights into key genes and mechanisms restoring photosynthetic efficiency in bread wheat (Triticum aestivum L.). Genomics 113:910–918

    Article  CAS  PubMed  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer W, Taiz AL, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cargnel MD, Demkura PV, Ballare CL (2014) Linking phytochrome to plant immunity: low red: far-red ratios increase Arabidopsis susceptibility to botrytis cinerea by reducing the biosynthesis of indolic glucosinolates and camalexin. New Phytol 204:342–354

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Chen L (2019) RNA-Seq analysis reveals differential responses of potato (Solanum tuberosum L.) plantlets cultured in vitro to red, blue, green, and white light-emitting diodes (LEDs). J Plant Growth Regul 38:1412–1427

    Article  CAS  Google Scholar 

  • Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu XJ (2013) A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol Plant 6:1769–1780

    Article  CAS  PubMed  Google Scholar 

  • Christie JM, Jenkins GI (1996) UV-B and UV-A/blue light signal transduction pathways induce chalcone synthase gene expression in Arabidopsis cells. Plant Cell 8:1555–1567

    CAS  PubMed  PubMed Central  Google Scholar 

  • Devlin PF, Kay SA (2000) Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell 12:2499–2510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeWit M, Galvao VC, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol 67:513–537

    Article  CAS  Google Scholar 

  • Doughty J, Aljabri M, Scott RJ (2014) Flavonoids and the regulation of seed size in Arabidopsis. Biochem Soc Trans 42:364–369

    Article  CAS  PubMed  Google Scholar 

  • Fuglevand G, Jackson JA, Jenkins GI (1996) UV-B, UV-A, and blue light signal transduction pathways interact synergistically to regulate chalcone synthase gene expression in Arabidopsis. Plant Cell 8:2347–2357

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gasperl A, Balogh E, Boldizsár Á, Kemeter N, Pirklbauer R, Möstl SB, Müller M, Zellnig G (2021) Comparison of light condition-dependent differences in the accumulation and subcellular localization of glutathione in Arabidopsis and wheat. Int J Mol Sci 22:607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gfeller A, Dubugnon L, Liechti R, Farmer EE (2010) Jasmonate biochemical pathway. Sci Signal 3:cm3

    PubMed  Google Scholar 

  • Goins GDB, Yorio NC, Sanwo MM, Brown CS (1997) Photomorphogenesis, photosynthesis, and seed yield of wheat plants grown under red light-emitting diodes (LEDs) with and without supplemental blue lighting. J Exp Bot 48:1407–1413

    Article  CAS  PubMed  Google Scholar 

  • Grieco M, Roustan V, Dermendjiev G, Rantala S, Jain A, Leonardelli M, Neumann K (2020) Adjustment of photosynthetic activity to drought and fluctuating light in wheat. Plant Cell Environ 43:1484–1500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinrich M, Hettenhausen C, Lange T (2013) High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems. Plant J 73:591–606

    Article  CAS  PubMed  Google Scholar 

  • Hua X, Wen C, Tian Y (2018) Spatio-temporal profiling of abscisic acid, indoleacetic acid and jasmonic acid in single rice seed during seed germination. Anal Chim Acta 15:119–127

    Google Scholar 

  • Ikeuchi M, Iwase A, Rymen B (2017) Wounding triggers callus formation via dynamic hormonal and transcriptional changes. Plant Physiol 175:1158–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:1182–1187

    Article  Google Scholar 

  • Kazan K, Manners JM (2011) The interplay between light and jasmonate signalling during defence and development. J Exp Bot 62:4087–4010

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Langmead B, Salzberg S (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohl M, Wiese S, Warscheid B (2011) Cytoscape: software for visualization and analysis of biological networks. Methods Mol Biol 696:291–303

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Khurana A, Sharma AK (2014) Role of plant hormones and their interplay in development and ripening of fleshy fruits. J Exp Bot 65:4561–4575

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landi M, Zivcak M, Sytar O, Brestic M, Allakhverdiev SI (2020) Plasticity of photosynthetic processes and the accumulation of secondary metabolites in plants in response to monochromatic light environments: a review. Biochim Biophys Acta Bioenerg 2:148131

    Article  Google Scholar 

  • Lgi A, Bhm B, Lv C (2020) The role of monochromatic red and blue light in tomato early photomorphogenesis and photosynthetic traits. Environ Exp Bot 179:104195

    Article  Google Scholar 

  • Liao Y, Smyth GK, Shi W (2015) FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930

    Article  Google Scholar 

  • Liu Y, Hou J, Wang X, Li T, Majeed U, Hao C, Zhang X (2020) The NAC transcription factor NAC019-A1 is a negative regulator of starch synthesis in wheat developing endosperm. J Exp Bot 7:5794–5807

    Article  Google Scholar 

  • Ma L (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machado RAR, Baldwin IT, Erb M (2017) Herbivory-induced jasmonates constrain plant sugar accumulation and growth by antagonizing gibberellin signaling and not by promoting secondary metabolite production. New Phytol 215:803–812

    Article  CAS  PubMed  Google Scholar 

  • Maloney GS, DiNapoli KT, Muday GK (2014) The anthocyanin reduced tomato mutant demonstrates the role of flavonols in tomato lateral root and root hair development. Plant Physiol 166:614–631

    Article  PubMed  PubMed Central  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793

    Article  CAS  PubMed  Google Scholar 

  • Meldau S, Erb M, Baldwin IT (2012) Defence on demand: mechanisms behind optimal defence patterns. Ann Bot 110:1503–1514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Millet E, Pinthus MJ (1984) Effects of removing floral organs, light penetration and physical constraint on the development of wheat grains. Ann Bot 53:261–269

    Article  Google Scholar 

  • Moreno JE, Tao Y, Chory J (2009) Ecological modulation of plant defense via control of jasmonate sensitivity. Proc Natl Acad Sci USA 106:4935–4940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mortazavi A, Williams B, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Ni J, Zhao Y, Tao R (2020) Ethylene mediates the branching of the jasmonate-induced flavonoid biosynthesis pathway by suppressing anthocyanin biosynthesis in red chinese pear fruits. Plant Biotechnol J 18:1223–1240

    Article  CAS  PubMed  Google Scholar 

  • Paul P, Singh SK, Patra B, Liu X, Pattanaik S, Yuan L (2020) Mutually regulated AP2/ERF gene clusters modulate biosynthesis of specialized metabolites in plants. Plant Physiol 182:840–856

    Article  CAS  PubMed  Google Scholar 

  • Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PlanTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:822–827

    Article  Google Scholar 

  • Pham MD, Hwang H, Park SW, Cui M, Lee H, Chun C (2019) Leaf chlorosis, epinasty, carbohydrate contents and growth of tomato show different responses to the red/blue wavelength ratio under continuous light. Plant Physiol Biochem 141:477–486

    Article  PubMed  Google Scholar 

  • Ramírez-González RH, Borrill P, Lang D, Harrington SA (2018) The transcriptional landscape of polyploid wheat. Science 361:662–662

    Article  Google Scholar 

  • Seo S, Sano H, Ohashi Y (1999) Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell 11:289–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Šimura J, Antoniadi I, Široká J (2018) Plant hormonomics: multiple phytohormone profiling by targeted metabolomics. Plant Physiol 177:476–489

    Article  PubMed  PubMed Central  Google Scholar 

  • Smakowska E, Kong J, Busch W, Belkhadir Y (2016) Organ-specific regulation of growth-defense tradeoffs by plants. Curr Opin Plant Biol 29:129–137

    Article  CAS  PubMed  Google Scholar 

  • Tehrani PF, Majd A, Mahmoodzadeh H, Satari TN (2016) Effect of red and blue light-emitting diodes on germination, morphological and anatomical features of Brassica napus. Adv Stud Biol 8:173–180

    Article  Google Scholar 

  • Thagun C, Imanishi S, Kudo T et al (2016) Jasmonate-responsive ERF transcription factors regulate steroidal glycoalkaloid biosynthesis in tomato. Plant Cell Physiol 57:961–975

    Article  CAS  PubMed  Google Scholar 

  • Ullmann-Zeunert L, Stanton MA, Wielsch N (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297

    Article  Google Scholar 

  • Wade HK, Bibikova TN, Valentine WJ, Jenkins GI (2001) Interactions within a network of phytochrome, cryptochrome and UV-B phototransduction pathways regulate chalcone synthase gene expression in Arabidopsis leaf tissue. Plant J 25:675–685

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Gu M, Cui J, Shi K, Zhou Y, Yu J (2009) Effects of light quality on CO2 assimilation, chlorophyll-fluorescence quenching, expression of calvin cycle genes and carbohydrate accumulation in Cucumis sativus. J Photochem Photobiol B 7:30–37

    Article  Google Scholar 

  • Wang R, Shu P, Zhang C, Zhang J, Chen Y, Zhang Y, Du K, Xie Y, Li M, Ma T, Zhang Y, Li Z, Grierson D (2022) Integrative analyses of metabolome and genome-wide transcriptome reveal the regulatory network governing flavor formation in kiwifruit (Actinidia chinensis). New Phytol 233:373–389

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Chen H, Li T, Xu F, Mao Z, Cao X, Miao L, Du S, Hua J, Zhao J, Guo T, Kou S, Wang W, Yang HQ (2021) Blue light-dependent interactions of CRY1 with GID1 and DELLA proteins regulate gibberellin signaling and photomorphogenesis in Arabidopsis. Plant Cell 33:2375–2394

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamada Y, Sato F (2013) Transcription factors in alkaloid biosynthesis. Int Rev Cell Mol Biol 305:339–382

    Article  CAS  PubMed  Google Scholar 

  • Yoshii M, Yamazaki M, Rakwal R, Kishi-Kaboshi M, Miyao A, Hirochika H (2010) The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. Plant J 61:804–815

    Article  CAS  PubMed  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:14

    Article  Google Scholar 

  • Zhang Y, Butelli E, Alseekh S (2015) Multi-level engineering facilitates the production of phenylpropanoid compounds in tomato. Nat Commun 10:8635

    Article  Google Scholar 

  • Zhao C, Liu X, Gong Q, Cao J, Shen W, Yin X, Grierson D, Zhang B, Xu C, Li X, Chen K, Sun C (2021) Three AP2/ERF family members modulate flavonoid synthesis by regulating type IV chalcone isomerase in citrus. Plant Biotechnol J 19:671–688

    Article  CAS  PubMed  Google Scholar 

  • Zhong M, Zeng B, Tang D, Yang J, Qu L, Yan J, Wang X, Li X, Liu X, Zhao X (2021) The blue light receptor CRY1 interacts with GID1 and DELLA proteins to repress GA signaling during photomorphogenesis in Arabidopsis. Mol Plant 14:1328–1342

    Article  CAS  PubMed  Google Scholar 

  • Zhou M, Memelink J (2016) Jasmonate-responsive transcription factors regulating plant secondary metabolism. Biotech Adv 34:441–449

    Article  Google Scholar 

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Acknowledgements

This work was supported by Major Program of National Agricultural Science and Technology of China (NK20220607), National Natural Science Foundation of China (31560388), and Yunnan Expert Workstation (202205AF150001). We thank the staff of Wuhan Metware Biotechnology Co., Ltd. (Wuhan, China), for their support during the metabolite data analysis. We would like to thank Editage (www.editage.cn) for English language editing.

Funding

This work was supported by Major Program of National Agricultural Science and Technology of China (NK20220607), National Natural Science Foundation of China (31560388), and Yunnan Expert Workstation (202205AF150001).

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Author notes

  1. Ping Zhang, Yongsheng Tang, Yongjiang Liu have contributed equally to this work.

Authors and Affiliations

  1. College of Agronomy and Biotechnology, Yunnan Agricultural University, Kunming, 650201, People’s Republic of China

    Ping Zhang, Yongjiang Liu, Junna Liu, Qianchao Wang, Hongxin Wang, Hanxue Li, Li Li & Peng Qin

  2. Qujing Academy of Agricultural Science, Qujing, 655000, People’s Republic of China

    Yongsheng Tang

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  1. Ping Zhang
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Contributions

PZ: Writing—original draft, methodology. YST: Conceptualization, writing—review and editing. YJL: Formal analysis, methodology. JNL and QCW: Data curation, visualization. LL: Data curation, investigation. HXL: Methodology, visualization. HXW: Formal analysis, investigation. PQ: Supervision, project administration, funding acquisition. All authors contributed to the discussion and approved the final paper. All authors endorse the final version of the manuscript.

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Correspondence to Peng Qin.

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Zhang, P., Tang, Y., Liu, Y. et al. Metabolic characteristics of self-pollinated wheat seed under red and blue light during early development. Planta 258, 63 (2023). https://doi.org/10.1007/s00425-023-04217-w

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