Domestication has altered the ABA and gibberellin profiles in developing pea seeds

. 2023 Jun 23 ; 258 (2) : 25. [epub] 20230623

Jazyk angličtina Země Německo Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37351659

Grantová podpora
19-07155S Grantová Agentura České Republiky
CZ.02.1.01/0.0/0.0/16_019/0000738 European Regional Development Fund Project "Centre for Experimental Plant Biology
CZ.02.1.01/0.0/0.0/16_019/0000827 Fundación de la Universidad Nacional del Comahue para el Desarrollo Regional

Odkazy

PubMed 37351659
PubMed Central PMC10290032
DOI 10.1007/s00425-023-04184-2
PII: 10.1007/s00425-023-04184-2
Knihovny.cz E-zdroje

We showed that wild pea seeds contained a more diverse combination of bioactive GAs and had higher ABA content than domesticated peas. Although the role of abscisic acid (ABA) and gibberellins (GAs) interplay has been extensively studied in Arabidopsis and cereals models, comparatively little is known about the effect of domestication on the level of phytohormones in legume seeds. In legumes, as in other crops, seed dormancy has been largely or entirely removed during domestication. In this study, we have measured the endogenous levels of ABA and GAs comparatively between wild and domesticated pea seeds during their development. We have shown that wild seeds contained more ABA than domesticated ones, which could be important for preparing the seeds for the period of dormancy. ABA was catabolised particularly by an 8´-hydroxylation pathway, and dihydrophaseic acid was the main catabolite in seed coats as well as embryos. Besides, the seed coats of wild and pigmented cultivated genotypes were characterised by a broader spectrum of bioactive GAs compared to non-pigmented domesticated seeds. GAs in both seed coat and embryo were synthesized mainly by a 13-hydroxylation pathway, with GA29 being the most abundant in the seed coat and GA20 in the embryos. Measuring seed water content and water loss indicated domesticated pea seeds´ desiccation was slower than that of wild pea seeds. Altogether, we showed that pea domestication led to a change in bioactive GA composition and a lower ABA content during seed development.

Zobrazit více v PubMed

Ali F, Qanmber G, Li F, Wang Z. Updated role of ABA in seed maturation, dormancy, and germination. J Adv Res. 2022;35:199–214. doi: 10.1016/j.jare.2021.03.011. PubMed DOI PMC

Alseekh S, Scossa F, Wen W, Luo J, Yan J, Beleggia R, Klee HJ, Huang S, Papa R, Fernie AR. Domestication of crop metabolomes: desired and unintended consequences. Trends Plant Sci. 2021;26(6):650–661. doi: 10.1016/j.tplants.2021.02.005. PubMed DOI

An JP, Yao JF, Xu RR, You CX, Wang XF, Hao YJ. Apple bZIP transcription factor MdbZIP44 regulates abscisic acid-promoted anthocyanin accumulation. Plant Cell Environ. 2018;41:2678–2692. doi: 10.1111/pce.13393. PubMed DOI

Balarynová J, Klčová B, Sekaninová J, Kobrlová L, Cechová MZ, Krejčí P, Leonova T, Gorbach D, Ihling C, Smržová L, Trněný O, Frolov A, Bednář P, Smýkal P. The loss of polyphenol oxidase function is associated with hilum pigmentation and has been selected during pea domestication. New Phytol. 2022;235:1807–1821. doi: 10.1111/nph.18256. PubMed DOI

Ben-Abu Y, Itsko M. Metabolome dynamics during wheat domestication. Sci Rep. 2022;12:1–9. doi: 10.1038/s41598-022-11952-9. PubMed DOI PMC

Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H. Development and aturation. In: Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H, editors. Seeds: physiology of development, germination and dormancy. 3. New York: Springer; 2013. pp. 27–83.

Cechová M, Válková M, Hradilová I, Janská A, Soukup A, Smýkal P, Bednář P. Towards better understanding of pea seed dormancy using laser desorption/ionization mass spectrometry. Int J Mol Sci. 2017;18:2196. doi: 10.3390/ijms18102196. PubMed DOI PMC

Corbineau F, Picard M, Fougereux J, Ladonne F, Côme D. Effects of dehydration conditions on desiccation tolerance of developing pea seeds as related to oligosaccharide content and cell membrane properties. Seed Sci Res. 2000;10:329–339. doi: 10.1017/S0960258500000374. DOI

Corcoran MR, Geissman TA, Phinney BO. Tannins as gibberellin antagonists. Plant Physiol. 1972;49:323–330. doi: 10.1104/pp.49.3.323. PubMed DOI PMC

Dong Z, Xiao Y, Govindarajulu R, Feil R, Siddoway ML, Nielsen T, Lunn JE, Hawkins J, Whipple C, Chuck G. The regulatory landscape of a core maize domestication module controlling bud dormancy and growth repression. Nat Commun. 2019;10:3810. doi: 10.1038/s41467-019-11774-w. PubMed DOI PMC

Ellis RH, Hong TD, Roberts EH. The development of desiccation-tolerance and maximum seed quality during seed maturation in six grain legumes. Ann Bot. 1987;59(1):23–29. doi: 10.1093/oxfordjournals.aob.a087280. DOI

Fernández-Marín B, Milla R, Martín-Robles N, Arc E, Kranner I, Becerril JM, García-Plazaola JI. Side-effects of domestication: cultivated legume seeds contain similar tocopherols and fatty acids but less carotenoids than their wild counterparts. BMC Plant Biol. 2014;14:1599. doi: 10.1186/s12870-014-0385-1. PubMed DOI PMC

Feurtado JA, Kermode AR. A merging of paths: abscisic acid and hormonal cross-talk in the control of seed dormancy maintenance and alleviation. In: Bradford K, Nonogaki H, editors. Annual plant reviews: seed development, dormancy and germination. Oxford: Blackwell Publishing Ltd; 2007. pp. 176–223.

Figueiredo DD, Batista RA, Roszak PJ, Hennig L, Köhler C. Auxin production in the endosperm drives seed coat development in Arabidopsis. Elife. 2016;5:e20542. doi: 10.7554/eLife.20542. PubMed DOI PMC

Frey A, Boutin J-P, Sotta B, Mercier R, Marion-Poll A. Regulation of carotenoid and ABA accumulation during the development and germination of Nicotiana plumbaginifolia seeds. Planta. 2006;224:622–632. doi: 10.1007/s00425-006-0231-2. PubMed DOI

Garcia-Martinez JL, Sponsel VM, Gaskin P. Gibberellins in developing fruits of Pisum sativum cv. Alaska:studies on their role in pod growth and seed development. Planta. 1987;170:130–137. doi: 10.1007/BF00392389. PubMed DOI

Graebe JE. Gibberellin biosynthesis and control. Annu Rev Plant Physiol. 1987;38:419–465. doi: 10.1146/annurev.pp.38.060187.002223. DOI

Green FB, Corcoran MR. Inhibitory action of five tannins on growth induced by several gibberellins. Plant Physiol. 1975;56:801–806. doi: 10.1104/pp.56.6.801. PubMed DOI PMC

Hedden P, Thomas SG. Gibberellin biosynthesis and its regulation. Biochem J. 2012;444:11–25. doi: 10.1042/BJ20120245. PubMed DOI

Hedley CL, Ambrose MJ. An analysis of seed development in Pisum sativum L. Ann Bot. 1980;46:89–105. doi: 10.1093/oxfordjournals.aob.a085900. DOI

Hradilová I, Trněný O, Válková M, Cechová M, Janská A, Prokešová L, Aamir K, Krezdorn N, Rotter B, Winter P, Varshney RK, Soukup A, Bednář P, Hanáček P, Smýkal P. A combined comparative transcriptomic, metabolomic, and anatomical analyses of two key domestication traits: Pod dehiscence and seed dormancy in pea (Pisum sp.) Front Plant Sci. 2017;8:542. doi: 10.3389/fpls.2017.00542. PubMed DOI PMC

Hsu FC. Abscisic acid accumulation in developing seeds of Phaseolus vulgaris L. Plant Physiol. 1979;63:552–556. doi: 10.1104/pp.63.3.552. PubMed DOI PMC

Jaakola L. New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci. 2013;18:477–483. doi: 10.1016/j.tplants.2013.06.003. PubMed DOI

Janská A, Pecková E, Sczepaniak B, Smýkal P, Soukup A. The role of the testa during the establishment of physical dormancy in the pea seed. Ann Bot. 2019;123:815–829. doi: 10.1093/aob/mcy213. PubMed DOI PMC

Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, Shen YY. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol. 2011;157:188–199. doi: 10.1104/pp.111.177311. PubMed DOI PMC

Jia L, Wu Q, Ye N, Liu R, Shi L, Xu W, Zhi H, Rahman ANMRB, Xia Y, Zhang J. Proanthocyanidins inhibit seed germination by maintaining a high level of abscisic acid in Arabidopsis thaliana. J Integ Plant Biol. 2012;54:663–673. doi: 10.1111/j.1744-7909.2012.01142.x. PubMed DOI

Karppinen K, Tegelberg P, Häggman H, Jaakola L. Abscisic acid regulates anthocyanin biosynthesis and gene expression associated with cell wall modification in ripening bilberry (Vaccinium myrtillus L.) fruits. Front Plant Sci. 2018;9:1259. doi: 10.3389/fpls.2018.01259. PubMed DOI PMC

Karssen CM, Brinkhorst-van der Swan DLC, Breekland AE, Koornneef M. Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. Planta. 1983;157:158–165. doi: 10.1007/BF00393650. PubMed DOI

King RW. Abscisic acid in developing wheat grains and its relationship to grain growth and maturation. Planta. 1976;132:43–51. doi: 10.1007/BF00390329. PubMed DOI

Krejčí P, Cechová MZ, Nádvorníková J, Barták P, Kobrlová L, Balarynová J, Smýkal P, Bednář P. Combination of electronically driven micromanipulation with laser desorption ionization mass spectrometry–The unique tool for analysis of seed coat layers and revealing the mystery of seed dormancy. Talanta. 2022;242:123303. doi: 10.1016/j.talanta.2022.123303. PubMed DOI

Kwak S-S, Kamiya Y, Sakurai A, Takahashi N. Isolation of a gibberellin biosynthesis inhibitor from testas of Phaseolus vulgaris L. Agric Biol Chem. 1988;52:149–151. doi: 10.1271/bbb1961.52.149. DOI

Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee I-J, Hwang I. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell. 2006;126:1109–1120. doi: 10.1016/j.cell.2006.07.034. PubMed DOI

Li G, Zhao J, Qin B, Yin Y, An W, Mu Z, Cao Y. ABA mediates development-dependent anthocyanin biosynthesis and fruit coloration in Lycium plants. BMC Plant Biol. 2019;19:1–13. doi: 10.1186/s12870-019-1931-7. PubMed DOI PMC

Liu Y, Fang J, Xu F, Chu J, Yan C, Schläppi MR, Wang Y, Chu C. Expression patterns of ABA and GA metabolism genes and hormone levels during rice seed development and imbibition: a comparison of dormant and non-dormant rice cultivars. J Genet Genom. 2014;41:327–338. doi: 10.1016/j.jgg.2014.04.004. PubMed DOI

Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P. Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol. 2008;179:1004–1016. doi: 10.1111/j.1469-8137.2008.02511.x. PubMed DOI

Martínez AB, Lema V, Capparelli A, Anido FL, Benech-Arnold R, Bartoli CG. Differences in seed dormancy associated with the domestication of Cucurbita maxima: elucidation of some mechanisms behind this response. Seed Sci Res. 2018;28(1):1–7. doi: 10.1017/S0960258517000320. DOI

Matthews S. Changes in developing pea (Pisum sativum) seeds in relation to their ability to withstand desiccation. Ann Appl Biol. 1973;75(1):93–105. doi: 10.1111/j.1744-7348.1973.tb01341.x. DOI

Mendoza MS, Dubreucq B, Miquel M, Caboche M, Lepiniec L. LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett. 2005;579:4666–4670. doi: 10.1016/j.febslet.2005.07.037. PubMed DOI

Nadeau CD, Ozga JA, Kurepin LV, Jin A, Pharis RP, Reinecke DM. Tissue-specific regulation of gibberellin biosynthesis in developing pea seeds. Plant Physiol. 2011;156:897–912. doi: 10.1104/pp.111.172577. PubMed DOI PMC

Nambara E, Marion-Poll A. ABA action and interactions in seeds. Trends Plant Sci. 2003;8:213–217. doi: 10.1016/S1360-1385(03)00060-8. PubMed DOI

Ney B, Duthion C, Fontaine E. Timing of reproductive abortions in relation to cell division, water content, and growth of pea seeds. Crop Sci. 1993;33(2):267–270. doi: 10.2135/cropsci1993.0011183X003300020010x. DOI

North HM, Almeida AD, Boutin J-P, Frey A, To A, Botran L, Sotta B, Marion-Poll A. The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. Plant J. 2007;50:810–824. doi: 10.1111/j.1365-313X.2007.03094.x. PubMed DOI

Ochatt SJ. Agroecological impact of an in vitro biotechnology approach of embryo development and seed filling in legumes. Agron Sustain Dev. 2015;35(2):535–552. doi: 10.1007/s13593-014-0276-8. DOI

Ochatt S, Abirached-Darmency M. The underlying processes governing seed size plasticity: impact of endoploidy on seed coat development and cell expansion in Medicago truncatula. In: de Bruin FJ, editor. The model legume Medicago truncatula. London: Wiley; 2019. pp. 99–116.

Paauw M, Koes R, Quattrocchio FM. Alteration of flavonoid pigmentation patterns during domestication of food crops. J Exp Bot. 2019;70:3719–3735. doi: 10.1093/jxb/erz141. PubMed DOI

Ranathunge K, Shao S, Qutob D, Gijzen M, Peterson CA, Bernards MA. Properties of the soybean seed coat cuticle change during development. Planta. 2010;231:1171–1188. doi: 10.1007/s00425-010-1118-9. PubMed DOI

Reinecke DM, Wickramarathna AD, Ozga JA, Kurepin LV, Jin AL, Good AG, Pharis RP. Gibberellin 3-oxidase gene expression patterns influence gibberellin biosynthesis, growth, and development in pea. Plant Physiol. 2013;163:929–945. doi: 10.1104/pp.113.225987. PubMed DOI PMC

Ribalta FM, Pazos-Navarro M, Nelson K, Edwards K, Ross JJ, Bennett RG, Munday C, Erskine W, Ochatt SJ, Croser JS. Precocious floral initiation and identification of exact timing of embryo physiological maturity facilitate germination of immature seeds to truncate the lifecycle of pea. Plant Growth Regul. 2017;81:345–353. doi: 10.1007/s10725-016-0211-x. DOI

Ribalta FM, Pazos-Navarro M, Edwards K, Ross JJ, Croser JS, Ochatt SJ. Expression patterns of key hormones related to pea (Pisum sativum L.) embryo physiological maturity shift in response to accelerated growth conditions. Front Plant Sci. 2019;10:1154. doi: 10.3389/fpls.2019.01154. PubMed DOI PMC

Rittenberg D, Foster GL. A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. J Biol Chem. 1940;133:737–744. doi: 10.1016/S0021-9258(18)73304-8. DOI

Schwartz SH, Zeevaart JAD. Abscisic acid biosynthesis and metabolism. In: Davies PJ, editor. Plant hormones: biosynthesis, signal transduction, action! Netherlands, Dordrecht: Springer; 2010. pp. 137–155.

Siegel S, Castellan NJ. Non parametric statistics for the behavioural sciences. New York: MacGraw Hill Int; 1988. pp. 213–214.

Smýkal P, Vernoud V, Blair MW, Soukup A, Thompson RD. The role of the testa during development and in establishment of dormancy of the legume seed. Front Plant Sci. 2014;5:351. doi: 10.3389/fpls.2014.00351. PubMed DOI PMC

Smýkal P, Nelson MN, Berger JD, Von Wettberg EJB. The Impact of genetic changes during crop domestication. Agronomy. 2018;8:119. doi: 10.3390/agronomy8070119. DOI

Sponsel VM. The localization, metabolism and biological activity of gibberellins in maturing and germinating seeds of Pisum sativum cv. Progress No. 9. Planta. 1983;159:454–468. doi: 10.1007/BF00392082. PubMed DOI

Tarkowská D, Strnad M. Isoprenoid-derived plant signaling molecules: biosynthesis and biological importance. Planta. 2018;247:1051–1066. doi: 10.1007/s00425-018-2878-x. PubMed DOI

Turečková V, Novák O, Strnad M. Profiling ABA metabolites in Nicotiana tabacum L. leaves by ultra-performance liquid chromatography–electrospray tandem mass spectrometry. Talanta. 2009;80:390–399. doi: 10.1016/j.talanta.2009.06.027. PubMed DOI

Urbanová T, Tarkowská D, Novák O, Hedden P, Strnad M. Analysis of gibberellins as free acids by ultra performance liquid chromatography–tandem mass spectrometry. Talanta. 2013;112:85–94. doi: 10.1016/j.talanta.2013.03.068. PubMed DOI

Van Dongen JT, Ammerlaan AM, Wouterlood M, Van Aelst AC, Borstlap AC. Structure of the developing pea seed coat and the post-phloem transport pathway of nutrients. Ann Bot. 2003;91:729–737. doi: 10.1093/aob/mcg066. PubMed DOI PMC

Wan L, Li B, Pandey MK, Wu Y, Lei Y, Yan L, Dai X, Jiang H, Zhang J, Wei G, Varshney RK, Liao B. Transcriptome analysis of a new peanut seed coat mutant for the physiological regulatory mechanism involved in seed coat cracking and pigmentation. Front Plant Sci. 2016;7:1491. doi: 10.3389/fpls.2016.01491. PubMed DOI PMC

Wang M, Li W, Fang C, Xu F, Liu Y, Wang Z, Yang R, Zhang M, Liu S, Lu S, Lin T, Tang J, Wang Y, Wang H, Lin H, Zhu B, Chen M, Kong F, Liu B, Zeng D, Jackson SA, Chu C, Tian Z. Parallel selection on a dormancy gene during domestication of crops from multiple families. Nat Genet. 2018;50:1435–1441. doi: 10.1038/s41588-018-0229-2. PubMed DOI

Weber H, Borisjuk L, Wobus U. Molecular physiology of legume seed development. Annu Rev Plant Biol. 2005;56:253–279. doi: 10.1146/annurev.arplant.56.032604.144201. PubMed DOI

Xie X-B, Li S, Zhang R-F, Zhao J, Chen Y-C, Zhao Q, Yao Y-X, You C-X, Zhang X-S, Hao Y-J. The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ. 2012;35:1884–1897. doi: 10.1111/j.1365-3040.2012.02523.x. PubMed DOI

Yamaguchi S. Gibberellin metabolism and its regulation. Annu Rev Plant Biol. 2008;59:225–251. doi: 10.1146/annurev.arplant.59.032607.092804. PubMed DOI

Zablatzká L, Balarynová J, Klčová B, Kopecký P, Smýkal P. Anatomy and histochemistry of seed coat development of wild (Pisum sativum subsp. elatius (M. Bieb.) Asch. et Graebn. and domesticated pea (Pisum sativum subsp. sativum L.) Int J Mol Sci. 2021;22:4602. doi: 10.3390/ijms22094602. PubMed DOI PMC

Zhao L, Li M, Ma X, Luo D, Zhou Q, Liu W, Liu Z. Transcriptome analysis and identification of abscisic acid and gibberellin-related genes during seed development of alfalfa (Medicago sativa L.) BMC Genom. 2022;23:651. doi: 10.1186/s12864-022-08875-0. PubMed DOI PMC

Zhou R, Cutler AJ, Ambrose SJ, Galka MM, Nelson KM, Squires TM, Loewen MK, Jadhav AS, Ross ARS, Taylor DC, Abrams SR. A new abscisic acid catabolic pathway. Plant Physiol. 2004;134:361–369. doi: 10.1104/pp.103.030734. PubMed DOI PMC

Zhu YX, Davies PJ, Halinska A. Metabolism of gibberellin A12 and A12-aldehyde in developing seeds of Pisum sativum L. Plant Physiol. 1991;97:26–33. doi: 10.1104/pp.97.1.26. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...