A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution
Yosuke Okanoa,1, Naoki Aonoa,1, Yuji Hiwatashia,b, Takashi Murataa,b, Tomoaki Nishiyamac,d, Takaaki Ishikawaa, Minoru Kuboc and Mitsuyasu Hasebea,b,c,2
+ Author Affiliations
aNational Institute for Basic Biology, Okazaki 444-8585, Japan;
bSchool of Life Science, The Graduate University for Advanced Studies, Okazaki 444-8585, Japan;
cERATO, Japan Science and Technology Agency, Okazaki 444-8585, Japan; and
dAdvanced Science Research Center, Kanazawa University, Kanazawa 920-0934, Japan
↵1Y.O. and N.A. contributed equally to this work.
Edited by Peter R. Crane, The University of Chicago, Chicago, IL, and approved July 27, 2009 (received for review June 22, 2009)
Abstract
Land plants have distinct developmental programs in haploid (gametophyte) and diploid (sporophyte) generations. Although usually the two programs strictly alternate at fertilization and meiosis, one program can be induced during the other program. In a process called apogamy, cells of the gametophyte other than the egg cell initiate sporophyte development. Here, we report for the moss Physcomitrella patens that apogamy resulted from deletion of the gene orthologous to the Arabidopsis thaliana CURLY LEAF (PpCLF), which encodes a component of polycomb repressive complex 2 (PRC2). In the deletion lines, a gametophytic vegetative cell frequently gave rise to a sporophyte-like body. This body grew indeterminately from an apical cell with the character of a sporophytic pluripotent stem cell but did not form a sporangium. Furthermore, with continued culture, the sporophyte-like body branched. Sporophyte branching is almost unknown among extant bryophytes. When PpCLF was expressed in the deletion lines once the sporophyte-like bodies had formed, pluripotent stem cell activity was arrested and a sporangium-like organ formed. Supported by the observed pattern of PpCLF expression, these results demonstrate that, in the gametophyte, PpCLF represses initiation of a sporophytic pluripotent stem cell and, in the sporophyte, represses that stem cell activity and induces reproductive organ development. In land plants, branching, along with indeterminate apical growth and delayed initiation of spore-bearing reproductive organs, were conspicuous innovations for the evolution of a dominant sporophyte plant body. Our study provides insights into the role of PRC2 gene regulation for sustaining evolutionary innovation in land plants.
branching PRC2 protracheophytes
Footnotes
2To whom correspondence should be addressed. E-mail: mhasebe@nibb.ac.jp
Author contributions: Y.O., N.A., Y.H., and M.H. designed research; Y.O., N.A., Y.H., T.M., T.N., T.I., and M.H. performed research; M.K. contributed new reagents/analytic tools; Y.O., N.A., Y.H., and M.H. analyzed data; and Y.O., T.M., M.K., and M.H. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
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