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A single homeobox gene triggers phase transition, embryogenesis and asexual reproduction

Abstract

Plants characteristically alternate between haploid gametophytic and diploid sporophytic stages. Meiosis and fertilization respectively initiate these two different ontogenies1. Genes triggering ectopic embryo development on vegetative sporophytic tissues are well described2,3; however, a genetic control of embryo development from gametophytic tissues remains elusive. Here, in the moss Physcomitrella patens we show that ectopic overexpression of the homeobox gene BELL1 induces embryo formation and subsequently reproductive diploid sporophytes from specific gametophytic cells without fertilization. In line with this, BELL1 loss-of-function mutants have a wild-type phenotype, except that their egg cells are bigger and unable to form embryos. Our results identify BELL1 as a master regulator for the gametophyte-to-sporophyte transition in P. patens and provide mechanistic insights into the evolution of embryos that can generate multicellular diploid sporophytes. This developmental innovation facilitated the colonization of land by plants about 500 million years ago4 and thus shaped our current ecosystems.

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Figure 1: Protein accumulation pattern of PpBELL1–GUS and PpBELL2–GUS during archegonia development and in the embryo determined by histochemical GUS assays.
Figure 2: Development of apogamous sporophytes on PpBELL1oe lines compared with WT sporophytes.
Figure 3: Morphological comparison of WT sporophytes and PpBELL1oe apogamous sporophytes.

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Acknowledgements

We thank J. Berman, P. Beyer, M. Lawton and G. Igloi for helpful comments on drafts of the manuscript, N. van Gessel for bioinformatic support, A. K. Prowse for proofreading and A. Novakovic for technical assistance. This work was supported by funds from the German-Israeli Foundation for Scientific Research and Development (GIF I-832-130.12/2004 and I-1008-154.13-2008 to N.O. and R.R.) and by the Excellence Initiative of the German Federal and State Governments (EXC294 to R.R.). I.P. was supported in part by a matching Tel-Aviv University Deans doctoral fellowship and the Manna foundation.

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Contributions

N.A.H. generated and analysed the PpBELL1oe lines and analysed the FIE/BELL1 double knockouts and MKN expression. A.K. generated and I.P. analysed the BELL1 knockouts; N.A.H. analysed sperms and egg cells of the BELL1 knockouts. A.K. generated and I.P., N.A.H. and N.O. analysed the BELL–GUS lines. A.K., N.A.H. and I.P. analysed BELL gene expression. A.K. and N.O. performed the BiFC experiments. N.A.H. performed additional analyses documented in Supplementary Figs 1, 2, 8 and 12. A.K., E.L.D., N.O. and R.R. planned and supervised the study. R.R., N.A.H. and N.O. wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Nir Ohad or Ralf Reski.

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Horst, N., Katz, A., Pereman, I. et al. A single homeobox gene triggers phase transition, embryogenesis and asexual reproduction. Nature Plants 2, 15209 (2016). https://doi.org/10.1038/nplants.2015.209

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