Maternal auxin supply contributes to early embryo patterning in Arabidopsis

Abstract

The angiosperm seed is composed of three genetically distinct tissues: the diploid embryo that originates from the fertilized egg cell, the triploid endosperm that is produced from the fertilized central cell, and the maternal sporophytic integuments that develop into the seed coat1. At the onset of embryo development in Arabidopsis thaliana, the zygote divides asymmetrically, producing a small apical embryonic cell and a larger basal cell that connects the embryo to the maternal tissue2. The coordinated and synchronous development of the embryo and the surrounding integuments, and the alignment of their growth axes, suggest communication between maternal tissues and the embryo. In contrast to animals, however, where a network of maternal factors that direct embryo patterning have been identified3,4, only a few maternal mutations have been described to affect embryo development in plants5,6,7. Early embryo patterning in Arabidopsis requires accumulation of the phytohormone auxin in the apical cell by directed transport from the suspensor8,9,10. However, the origin of this auxin has remained obscure. Here we investigate the source of auxin for early embryogenesis and provide evidence that the mother plant coordinates seed development by supplying auxin to the early embryo from the integuments of the ovule. We show that auxin response increases in ovules after fertilization, due to upregulated auxin biosynthesis in the integuments, and this maternally produced auxin is required for correct embryo development.

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Fig. 1: Auxin accumulation in integuments.
Fig. 2: Auxin biosynthesis mutants display early embryonic defects.
Fig. 3: Sporophytic maternal early embryonic defects.

References

  1. 1.

    Figueiredo, D. D. & Köhler, C. C. Auxin: a molecular trigger of seed development. Genes Dev. 32, 479–490 (2018).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  2. 2.

    Mansfield, S. G. & Briarty, L. G. Early embryogenesis in Arabidopsis thaliana. 2. The developing embryo. Can. J. Bot.-Rev. Can. De. Bot. 69, 461–476 (1991).

    Article  Google Scholar 

  3. 3.

    Johnstone, O. & Lasko, P. Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu. Rev. Genet. 35, 365–406 (2001).

    Article  PubMed  CAS  Google Scholar 

  4. 4.

    Riechmann, V. & Ephrussi, A. Axis formation during Drosophila oogenesis. Curr. Opin. Gen. Dev. 11, 374–383 (2001).

    Article  CAS  Google Scholar 

  5. 5.

    Ray, S., Golden, T. & Ray, A. Maternal effects of the short integument mutation on embryo development in. Arab. Dev. Biol. 180, 365–369 (1995).

    Article  Google Scholar 

  6. 6.

    Prigge, M. J. & Wagner, D. R. The Arabidopsis SERRATE gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 13, 1263–1280 (2001).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. 7.

    Costa, L. M. et al. Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 344, 168–172 (2014).

    Article  PubMed  CAS  Google Scholar 

  8. 8.

    Möller, B. K. & Weijers, D. Auxin control of embryo patterning. Cold Spring Harb. Perspect. Biol. 1, a001545 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. 9.

    Friml, J. et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 (2003).

    Article  PubMed  CAS  Google Scholar 

  10. 10.

    Robert, H. S. et al. Local auxin sources orient the apical-basal axis in Arabidopsis embryos. Curr. Biol. 23, 2506–2512 (2013).

    Article  PubMed  CAS  Google Scholar 

  11. 11.

    Brunoud, G. et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103–106 (2012).

    Article  PubMed  CAS  Google Scholar 

  12. 12.

    Liao, C.-Y. et al. Reporters for sensitive and quantitative measurement of auxin response. Nat. Methods 12, 207–210 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. 13.

    Paciorek, T. & Friml, J. Auxin signaling. J. Cell Sci. 119, 1199–1202 (2006).

    Article  PubMed  CAS  Google Scholar 

  14. 14.

    Ljung, K. Auxin metabolism and homeostasis during plant development. Development 140, 943–950 (2013).

    Article  PubMed  CAS  Google Scholar 

  15. 15.

    Stepanova, A. N. et al. The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23, 3961–3973 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. 16.

    Mashiguchi, K. et al. The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 18512–18517 (2011).

    Article  PubMed  Google Scholar 

  17. 17.

    Won, C. et al. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 18518–18523 (2011).

    Article  PubMed  Google Scholar 

  18. 18.

    Stepanova, A. N. et al. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133, 177–191 (2008).

    Article  PubMed  CAS  Google Scholar 

  19. 19.

    Jensen, P. J., Hangarter, R. P. & Estelle, M. Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol. 116, 455–462 (1998).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. 20.

    Debeaujon, I. et al. Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15, 2514–2531 (2003).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. 21.

    Figueiredo, D. D., Batista, R. A., Roszak, P. J., & Köhler, C. C. Auxin production couples endosperm development to fertilization. Nat. Plants 1, 15184 (2015).

    Article  PubMed  CAS  Google Scholar 

  22. 22.

    Figueiredo, D. D., Batista, R. A., Roszak, P. J., Hennig, L. & Köhler, C. C. Auxin production in the endosperm drives seed coat development in Arabidopsis. eLife 5, e20542 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Blilou, I. et al. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44 (2005).

    Article  PubMed  CAS  Google Scholar 

  24. 24.

    Vieten, A. et al. Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132, 4521–4531 (2005).

    Article  PubMed  CAS  Google Scholar 

  25. 25.

    Weijers, D. et al. Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10, 265–270 (2006).

    Article  PubMed  CAS  Google Scholar 

  26. 26.

    Larsson, E., Vivian-Smith, A., Offringa, R. & Sundberg, E. Auxin homeostasis in Arabidopsis ovules is anther-dependent at maturation and changes dynamically upon fertilization. Front. Plant Sci. 8, 315–14 (2017).

    Article  Google Scholar 

  27. 27.

    Weijers, D. et al. Maintenance of embryonic auxin distribution for apical-basal patterning by PIN-FORMED-dependent auxin transport in Arabidopsis. Plant Cell 17, 2517–2526 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. 28.

    Wabnik, K., Robert, H. S., Smith, R. S. & Friml, J. Modeling framework for the establishment of the apical-basal embryonic axis in plants. Curr. Biol. 23, 2513–2518 (2013).

    Article  PubMed  CAS  Google Scholar 

  29. 29.

    Prat, T. et al. WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity. PLoS Genet. 14, e1007177 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. 30.

    Gallavotti, A., Yang, Y., Schmidt, R. J. & Jackson, D. P. The relationship between auxin transport and maize branching. Plant Physiol. 147, 1913–1923 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. 31.

    Zhang, J., & Peer, W. A. Auxin homeostasis: the DAO of catabolism. J. Exp. Bot. 68, 3145–3154 (2017).

    Article  PubMed  CAS  Google Scholar 

  32. 32.

    Pencík, A. et al. Ultra-rapid auxin metabolite profiling for high-throughput mutant screening in Arabidopsis. J. Exp. Bot. 69, 2569–2579 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank E. Groot for assistance with statistical analyses and for critical reading of the manuscript. We thank J. Alonso for providing wei8-1, wei8-1 tar1-1, pDR5:GFP wei8-1, and pTAA1:GFP-TAA1 seeds, G. Jürgens for providing pDR5:nls-3xGFP and pDR5:nls-3xGFP wei8-1 tar1-1 seeds, T. Vernoux for p35S:DII-VENUS and p35S:mDII-VENUS seeds and plasmids, R. Offringa for pSDM7010 and pSDM7012, L. Lepiniec for pBAN-pBS-SK, C.-Y. Liao and D. Weijers for R2D2 seeds, and T. Friedrich for valuable suggestions. Seeds of wei8-3 and wei-11 seeds were obtained from the European Arabidopsis Stock Center (NASC). We acknowledge the CEITEC core facility CELLIM supported by the MEYS CR (LM2015062 Czech-BioImaging), and the CEITEC core facility Plant Sciences. H.S.R. was supported by the SoMoProII program co-financed by the South-Moravian Region and the European Union, by the Ministry of Education, Youth and Sports of the Czech Republic within CEITEC 2020 (LQ1601) and by the Masaryk University. C.P. was supported by the Kwanjeong Educational Foundation. C.L.G. was supported by the Deutscher Akademischer Austauschdienst. W.G. was a post-doctoral fellow of the Research Foundation Flanders. B.W. was supported by the ‘NITKA’ project under European Social Fund UDA-POKL.04.03.00-00-168/12, realized at the University of Silesia, Katowice, Poland. A.P and O.N. were supported by the Czech Foundation Agency (GA17-21581Y) and the Ministry of Education, Youth and Sports of the Czech Republic via the National Program for Sustainability (LO1204). J.C. is a post-doctoral fellow supported by a grant from the Deutsche Forschungsgemeinschaft (Dr334/10) to T.D. This work was further supported by the European Research Council (FP7/2007-2013 / ERC-grant agreement no. 282300 to J.F.), and the Czech Science Foundation GACR (GA13-40637S) to J.F.; and by the Deutsche Forschungsgemeinschaft (La606/6, La606/13, La606/17 and ERA-CAPS program), and the EU 7th framework program (ITN SIREN) to T.L. This material reflects only the author’s views and the European Union is not liable for any use that may be made of the information contained therein.

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H.S.R., C.P. and C.L.G. contributed equally to this work and performed experiments. H.S.R., B.W., A.P. and O.N. collected samples and performed the analysis for the auxin measurements. W.G. participated in the backcrosses experiments. J.C. and T.D. provided the maize data. H.S.R., C.P., C.L.G., J.F. and T.L. designed the experiments, analysed the data and wrote the paper.

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Correspondence to Hélène S. Robert or Jiří Friml or Thomas Laux.

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Impact statement:

Early embryo development requires auxin production in the surrounding maternal integuments.

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Supplementary Materials, Supplementary Figures 1–6, Supplementary Tables 1–3 and Supplementary References

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Robert, H.S., Park, C., Gutièrrez, C.L. et al. Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nature Plants 4, 548–553 (2018). https://doi.org/10.1038/s41477-018-0204-z

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