A role for auxin signaling in the acquisition of longevity during seed maturation.
ABSCISIC ACID INSENSITIVE3
Arabidopsis thaliana
auxin distribution
auxin signaling
longevity
maturation
seed
storage
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
18
06
2019
accepted:
14
08
2019
pubmed:
29
8
2019
medline:
12
11
2020
entrez:
29
8
2019
Statut:
ppublish
Résumé
Seed longevity, the maintenance of viability during dry storage, is a crucial factor to preserve plant genetic resources and seed vigor. Inference of a temporal gene-regulatory network of seed maturation identified auxin signaling as a putative mechanism to induce longevity-related genes. Using auxin-response sensors and tryptophan-dependent auxin biosynthesis mutants of Arabidopsis thaliana L., the role of auxin signaling in longevity was studied during seed maturation. DII and DR5 sensors demonstrated that, concomitant with the acquisition of longevity, auxin signaling input and output increased and underwent a spatiotemporal redistribution, spreading throughout the embryo. Longevity of seeds of single auxin biosynthesis mutants with altered auxin signaling activity was affected in a dose-response manner depending on the level of auxin activity. Longevity-associated genes with promoters enriched in auxin response elements and the master regulator ABSCISIC ACID INSENSITIVE3 were induced by auxin in developing embryos and deregulated in auxin biosynthesis mutants. The beneficial effect of exogenous auxin during seed maturation on seed longevity was abolished in abi3-1 mutants. These data suggest a role for auxin signaling activity in the acquisition of longevity during seed maturation.
Substances chimiques
ABI3 protein, Arabidopsis
0
Arabidopsis Proteins
0
Indoleacetic Acids
0
Transcription Factors
0
Abscisic Acid
72S9A8J5GW
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
284-296Informations de copyright
© 2019 INRA New Phytologist © 2019 New Phytologist Trust.
Références
Bai B, Novák O, Ljung K, Hanson J, Bentsink L. 2018. Combined transcriptome and translatome analyses reveal a role for tryptophan-dependent auxin biosynthesis in the control of DOG1-dependent seed dormancy. New Phytologist 217: 1077-1085.
Batista RA, Figueiredo DD, Santos-González J, Köhler C. 2019. Auxin regulates endosperm cellularization in Arabidopsis. Genes and Development 33: 466-476.
Bentsink L, Koornneef M. 2008. Seed dormancy and germination. Arabidopsis Book 6: e0119.
Biswas KK, Ooura C, Higuchi K, Miyazaki Y, Van Nguyen V, Rahman A, Uchimiya H, Kiyosue T, Koshiba T, Tanaka A et al. 2007. Genetic characterization of mutants resistant to the antiauxin p-chlorophenoxyisobutyric acid reveals that AAR3, a gene encoding a DCN1-like protein, regulates responses to the synthetic auxin 2,4-dichlorophenoxyacetic acid in Arabidopsis roots. Plant Physiology 145: 773-785.
Brady SM, Sarkar SF, Bonetta D, McCourt P. 2003. The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. The Plant Journal 34: 67-75.
Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ et al. 2012. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482: 103-106.
Bueso E, Muñoz-Bertomeu J, Campos F, Brunaud V, Martínez L, Sayas E, Ballester P, Yenush L, Serrano R. 2014. ARABIDOPSIS THALIANA HOMEOBOX25 uncovers a role for gibberellins in seed longevity. Plant Physiology 164: 999-1010.
Carranco R, Espinosa JM, Prieto-Dapena P, Almoguera C, Jordano J. 2010. Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factor-mediated seed longevity. Proceedings of the National Academy of Sciences, USA 107: 21908-21913.
Chatelain E, Hundertmark M, Leprince O, Le Gall S, Satour P, Deligny-Penninck S, Rogniaux H, Buitink J. 2012. Temporal profiling of the heat-stable proteome during late maturation of Medicago truncatula seeds identifies a restricted subset of late embryogenesis abundant proteins associated with longevity. Plant, Cell & Environment 35: 1440-1455.
Debeaujon I, Léon-Kloosterziel KM, Koornneef M. 2000. Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiology 122: 403-414.
Dekkers BJ, He H, Hanson J, Willems LA, Jamar DC, Cueff G, Rajjou L, Hilhorst HW, Bentsink L. 2016. The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. The Plant Journal 85: 451-465.
Delmas F, Sankaranarayanan S, Deb S, Widdup E, Bournonville C, Bollier N, Northey JG, McCourt P, Samuel MA. 2013. ABI3 controls embryo degreening through Mendel's I locus. Proceedings of the National Academy of Sciences, USA 110: 3888-3894.
Figueiredo DD, Batista RA, Roszak PJ, Hennig L, Köhler C. 2016. Auxin production in the endosperm drives seed coat development in Arabidopsis. eLife 5: e20542.
Figueirode DD, Köhler C. 2018. Auxin: a molecular trigger of seed development. Genes and Development 32: 479-490.
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G. 2003. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
Halder V, Kombrink E. 2015. Facile high-throughput forward chemical genetic screening by in situ monitoring of glucuronidase-based reporter gene expression in Arabidopsis thaliana. Frontiers in Plant Science 29: e13.
Hull AK, Vij R, Celenza JL. 2000. Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proceedings of the National Academy of Sciences, USA 97: 2379-2384.
Hundertmark M, Buitink J, Leprince O, Hincha DK. 2011. The reduction of seed-specific dehydrins reduces seed longevity in Arabidopsis thaliana. Seed Science Research 21: 165-173.
Jenik PD, Barton MK. 2005. Surge and destroy: the role of auxin in plant embryogenesis. Development 132: 3577-3585.
Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M. 2010. Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell and Physiology 51: 1988-2001.
Kanno Y, Oikawa T, Chiba Y, Ishimaru Y, Shimizu T, Sano N, Koshiba T, Kamiya Y, Ueda M, Seo M. 2016. AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nature Communications 7: e13245.
Kotak S, Vierling E, Bäumlein H, von Koskull-Döring P. 2007. A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19: 182-195.
Kranner I, Birtić S, Anderson KM, Pritchard HW. 2006. Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radical Biology & Medicine 40: 2155-2165.
Leprince O, Pellizzaro A, Berriri S, Buitink J. 2017. Late seed maturation: drying without dying. Journal of Experimental Botany 68: 827-841.
Leyser O. 2018. Auxin signaling. Plant Physiology 176: 465-479.
Liao CY, Smet W, Brunoud G, Yoshida S, Vernoux T, Weijers D. 2015. Reporters for sensitive and quantitative measurement of auxin response. Nature Methods 12: 207-210.
Liu L, Tong H, Xiao Y, Che R, Xu F, Hu B, Liang C, Chu J, Li J, Chu C. 2010. Activation of Big Grain1 significantly improves grain size by regulating auxin transport in rice. Proceedings of the National Academy of Sciences, USA 112: 11102-11107.
Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He ZH. 2013. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 110: 15485-15490.
Mikkelsen MD1, Hansen CH, Wittstock U, Halkier BA. 2000. Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. Journal of Biological Chemistry 275: 33712-33717.
Ooms J, Leon-Kloosterziel KM, Bartels D, Koornneef M, Karssen CM. 1993. Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana: a comparative study using abscisic acid-insensitive abi3 mutants. Plant Physiology 102: 1185-1191.
Panoli A, Martin MV, Alandete-Saez M, Simon M, Neff C, Swarup R, Bellido A, Yuan L, Pagnussat GC, Sundaresan V. 2015. Auxin import and local auxin biosynthesis are required for mitotic divisions, cell expansion and cell specification during female gametophyte development in Arabidopsis thaliana. PLoS ONE 10: e0126164.
Prieto-Dapena P, Castaño R, Almoguera C, Jordano J. 2006. Improved resistance to controlled deterioration in transgenic seeds. Plant Physiology 142: 1102-1112.
Rademacher EH, Lokerse AS, Schlereth A, Llavata-Peris CI, Bayer M, Kientz M, Freire Rios A, Borst JW, Lukowitz W, Jürgens G et al. 2012. Different auxin response machineries control distinct cell fates in the early plant embryo. Developmental Cell 22: 211-222.
Richards HA, Halfhill MD, Millwood RJ, Stewart CN. 2003. Quantitative GFP fluorescence as an indicator of recombinant protein synthesis in transgenic plants. Plant Cell Reports 22: 117-121.
Righetti K, Vu JL, Pelletier S, Vu BL, Glaab E, Lalanne D, Pasha A, Patel RV, Provart NJ, Verdier J et al. 2015. Inference of longevity-related genes from a robust coexpression network of seed maturation identifies regulators linking seed storability to biotic defense-related pathways. Plant Cell 27: 2692-2708.
Robert HS, Park C, Gutierrez CL, Wojcikowska B, Pencik A, Novak O, Chen J, Grunewald W, Dresselhaus T, Friml J et al. 2018. Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nature Plants 4: 548-553.
Rosnoblet C, Aubry C, Leprince O, Vu BL, Rogniaux H, Buitink J. 2007. The regulatory gamma subunit SNF4b of the sucrose non-fermenting-related kinase complex is involved in longevity and stachyose accumulation during maturation of Medicago truncatula seeds. The Plant Journal 51: 47-59.
Salehin M, Bagchi R, Estelle M. 2015. SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell 27: 9-19.
Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D. 2004. Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16: 1419-1432.
Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ. 2006. The ARF2 gene of Arabidopsis thaliana links auxin signaling cell division and the size of seeds and other organs. Development 113: 251-266.
Spiess GM, Hausman A, Yu P, Cohen JD, Rampey RA, Zolman BK. 2014. Auxin input pathway disruptions are mitigated by changes in auxin biosynthetic gene expression in Arabidopsis. Plant Physiology 165: 1092-1104.
Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jürgens G, Alonso JM. 2008. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133: 177-191.
Sugliani M, Rajjou L, Clerkx EJ, Koornneef M, Soppe WJ. 2009. Natural modifiers of seed longevity in the Arabidopsis mutants abscisic acid insensitive3-5 (abi3-5) and leafy cotyledon1-3 (lec1-3). New Phytologist 184: 898-908.
Verdier J, Lalanne D, Pelletier S, Torres-Jerez I, Righetti K, Bandyopadhyay K, Leprince O, Chatelain E, Vu BL, Gouzy J et al. 2013. A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds. Plant Physiology 163: 757-774.
Weijers D, Wagner D. 2016. Transcriptional responses to the auxin hormone. Annual Review of Plant Biology 29: 539-574.
Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL. 2002. Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes and Development 16: 3100-3112.
Zhou ZY, Zhang CG, Wu L, Zhang CG, Chai J, Wang M, Jha A, Jia PF, Cui SJ, Yang M et al. 2011. Functional characterization of the CKRC1/TAA1 gene and dissection of hormonal actions in the Arabidopsis root. The Plant Journal 66: 516-527.
Zinsmeister J, Lalanne D, Terrasson E, Chatelain E, Vandecasteele C, Vu BL, Dubois-Laurent C, Geoffriau E, Signor CL, Dalmais M et al. 2016. ABI5 is a regulator of seed maturation and longevity in legumes. Plant Cell 28: 2735-2754.