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A Polycomb Repressive Complex 2 Gene Regulates Apogamy and Gives Evolutionary Insights Into Early Land Plant Evolution

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A Polycomb Repressive Complex 2 Gene Regulates Apogamy and Gives Evolutionary Insights Into Early Land Plant Evolution 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 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 Edited by Peter R. Crane, The University of Chicago, Chicago, IL, and approved July 27, 2009 (received for review June 22, 2009) Land plants have distinct developmental programs in haploid ogy, development, and evolution (5–7), the gene regulatory (gametophyte) and diploid (sporophyte) generations. Although network remains undeciphered. usually the two programs strictly alternate at fertilization and Parthenogenetic development of egg cells has been observed meiosis, one program can be induced during the other program. In in some alleles of loss-of-function mutants of the Arabidopsis a process called apogamy, cells of the gametophyte other than the thaliana genes FERTILIZATION-INDEPENDENT SEED 2 egg cell initiate sporophyte development. Here, we report for the (FIS2), MEDEA (MEA), and MULTICOPY SUPPRESSOR OF moss Physcomitrella patens that apogamy resulted from deletion IRA 1 (MSI1) (8, 9), which encode members of the polycomb of the gene orthologous to the Arabidopsis thaliana CURLY LEAF repressive complex 2 (PRC2) (8, 10, 11). The PRC2 complex was (PpCLF), which encodes a component of polycomb repressive first characterized in Drosophila melanogaster as a regulator of complex 2 (PRC2). In the deletion lines, a gametophytic vegetative HOX genes and includes four core proteins: Extra sex comb cell frequently gave rise to a sporophyte-like body. This body grew (ESC), Enhancer of zeste [E(Z)], Suppressor of zeste 12 indeterminately from an apical cell with the character of a sporo- [SU(Z)12], and P55 (12). Orthologs of PRC2 genes were found phytic pluripotent stem cell but did not form a sporangium. in a wide range of organisms including land plants and this Furthermore, with continued culture, the sporophyte-like body complex dynamically mediates transcriptional silencing of nu- branched. Sporophyte branching is almost unknown among extant merous genes, based on modifying trimethylation of lysine 27 on bryophytes. When PpCLF was expressed in the deletion lines once histone H3 (12, 13). Several E(Z) and SU(Z)12 paralogs are the sporophyte-like bodies had formed, pluripotent stem cell coded in the A. thaliana genome and at least three distinct activity was arrested and a sporangium-like organ formed. Sup- complexes, with different combinations of the paralogs, have been implicated in plant development: the FIS complex in seed ported by the observed pattern of PpCLF expression, these results development including the prevention of parthenogenesis, the EVOLUTION demonstrate that, in the gametophyte, PpCLF represses initiation VERNALIZATION (VRN) complex in vernalization response, of a sporophytic pluripotent stem cell and, in the sporophyte, and the EMBRYONIC FLOWER (EMF) complex in flowering represses that stem cell activity and induces reproductive organ and flower development (14–16). development. In land plants, branching, along with indeterminate We sought to investigate the ancestral function and subse- apical growth and delayed initiation of spore-bearing reproductive quent evolution of the PRC2 complex in land plants, taking organs, were conspicuous innovations for the evolution of a advantage of the genomics (17), the feasibility of gene targeting, dominant sporophyte plant body. Our study provides insights into and the accessible development of the moss, Physcomitrella the role of PRC2 gene regulation for sustaining evolutionary patens. During the course of study, we found that deletion in P. innovation in land plants. patens of the gene orthologous to D. melanogaster E(Z) and A. thaliana CURLY LEAF (CLF)/MEA/SWINGER (SWN)(Pp- branching ͉ PRC2 ͉ protracheophytes CLF) induced unusual sporophyte-like bodies. Here, we report the characterization of the role of the PpCLF gene in P. patens evelopment of land plants starts from a zygote in the development, revealing multiple functions, including the repres- Dsporophyte generation and from a spore in the gametophyte sion of apogamy in the haploid generation, that bear on the generation. Although sporophyte development is usually pre- evolution of body plan in land plants. vented in the gametophyte until fertilization, it can occur naturally and be induced experimentally. Female gametes (egg Results cells) can initiate embryogenesis with parthenogenetic develop- Molecular Cloning of a CURLY LEAF Ortholog in Physcomitrella patens. ment in the absence of fertilization (1, 2). Additionally, in a A candidate cDNA sequence of PpCLF was obtained using the process called apogamy, somatic gametophyte cells are repro- A. thaliana CLF amino acid sequence (18) as the query for a grammed to start a sporophytic developmental program (3). While apogamy can be induced experimentally in flowering Author contributions: Y.O., N.A., Y.H., and M.H. designed research; Y.O., N.A., Y.H., T.M., plants from synergid and antipodal cells, this is rare and not T.N., T.I., and M.H. performed research; M.K. contributed new reagents/analytic tools; Y.O., known to happen naturally (4); in contrast, this type of asexual N.A., Y.H., and M.H. analyzed data; and Y.O., T.M., M.K., and M.H. wrote the paper. reproduction is more widely observed in non-seed plants, in- The authors declare no conflict of interest. cluding pteridophytes (5) and bryophytes (6). Bypassing game- This article is a PNAS Direct Submission. togenesis and fertilization, gametophyte somatic cells of non- Data deposition: The sequences reported in this paper have been deposited in the GenBank seed plants divide several times to form a sporophyte apical database (accession nos. AB472766). meristem including a pluripotent stem cell. Apogamy in these 1Y.O. and N.A. contributed equally to this work. species can be induced with exogenous factors, such as hydration, 2To whom correspondence should be addressed. E-mail: [email protected]. sugars, chloral hydrate, and phytohormones (6). Even though This article contains supporting information online at www.pnas.org/cgi/content/full/ apogamy has been well-studied from the viewpoints of physiol- 0906997106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0906997106 PNAS ͉ September 22, 2009 ͉ vol. 106 ͉ no. 38 ͉ 16321–16326 Downloaded by guest on September 30, 2021 TBLASTN search (19) against the P. patens subsp. patens v. 1.1 genome database. The PpCLF cDNA sequence was obtained by RT-PCR using gene-specific primers. With the sequenced ge- nome (17), we identified PpCLF as the sole homolog of the E(Z) component of PRC2 (Fig. S1). This component is represented in the A. thaliana genome by three genes, CLF, MEA, and SWN. PpCLF has the SET, CXC, and C5 domains as other E(Z) proteins have. The P. patens genome also includes homologues of the other members of the PRC2 complex (10, 20). Deletion of PpCLF Gene Induces Sporophyte-Like Body. Using gene targeting, we generated four deletion lines of PpCLF (ppclf-del-1 to -4) (Fig. S2), and the phenotypes of the lines were indistin- guishable from each other. Following spore germination in P. patens, a cell filament forms, known as a protonema, whose apical, or tip, cell has the characteristics of a pluripotent stem cell. When grown under red-light (21), in both wild-type and deletion lines, the apical cell continuously produced protonema cells (Fig. 1 A and B), although the chloroplasts in the deletion lines were smaller than those of the wild type. When red-light- grown wild-type protonemata were transferred to white light, the protonema cells formed side-branch initial cells that gave rise to protonema apical cells, which are pluripotent (Fig. 1C). In contrast, when red-light-grown PpCLF deletion lines were moved into white light, although side-branch initials formed, they gave rise to tissue that differed from protonemata (Fig. 1D). This tissue had a single apical cell with two faces, each producing a row of cells, with subsequent periclinal divisions forming inner and outer cell layers (Fig. 1 E and F). The development and three-dimensional cellular organization of this tissue is similar to those of a young sporophyte (22). The frequency of side branch formation of whatever fate was approximately similar in wild type and deletion lines, but while the fate of side-branch development in the wild type, as expected (23), could be effectively changed from protonema to gametophore by cytoki- nin, the fate of the sporophyte-like side branches in the deletion line remained unchanged on cytokinin (Table S1). Expression Patterns of MKN4 and PpLFY2 in the Sporophyte-Like Body Are Similar to Those of the Wild-Type Sporophyte. To examine whether side-branch initial cells are fated to form sporophyte apical cells instead of protonema or gametophore apical cells, we deleted the PpCLF gene in the MKN4-GUS-3 (22) and PpLFY2- GUS-1 (24) lines (Fig. S3). In the parental MKN4-GUS-3 line, the MKN4-GUS fusion protein is detected specifically in sporo- phyte apical cells but not in gametophyte apical cells (22). In a Fig. 1. A PpCLF deletion line (ppclf-del-3) forms sporophyte-like bodies as PpCLF deletion background, the MKN4-GUS signal was de- side branches. (A and B) Wild-type (A) and ppclf-del-3 (B) protonemata grown tected only in the apical cells of sporophyte-like tissue (Fig. 1G). under red light for 7 days. Asterisks and arrows indicate apical cells and septa, In the PpLFY2-GUS-1 line, GUS signal is present throughout respectively. (C and D) Protonema of the wild type (C) and ppclf-del-3 (D) the young sporophyte (24), similar to its appearance in the grown in white light for 2 days after 7 days of culture in red light.
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