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05 Vasc Pl II-Ferns.Pptx REPORTS share several characteristics with xylem vessels Contribution of NAC Transcription from vascular plants, such as an elongated shape and an absence of cellular contents (13). How- ever, unlike xylem vessels, hydroids lack distinct Factors to Plant Adaptation to Land pits on their lateral walls, and there is an absence of lignified secondary wall (14–17). Stereid cells Bo Xu,1 Misato Ohtani,2* Masatoshi Yamaguchi,1† Kiminori Toyooka,2 Mayumi Wakazaki,2 have thickened cell walls and are hypothesized to Mayuko Sato,2 Minoru Kubo,3‡ Yoshimi Nakano,1 Ryosuke Sano,1 Yuji Hiwatashi,3§ function as supporting elements (18). Both hydroids Takashi Murata,3 Tetsuya Kurata,1 Arata Yoneda,1 Ko Kato,1 Mitsuyasu Hasebe,3,4 Taku Demura1,2* and stereids are formed mainly in the gameto- The development of cells specialized for water conduction or support is a striking innovation of plants phytic generation, unlike xylem vessels and fiber that has enabled them to colonize land. The NAC transcription factors regulate the differentiation of cells, which are formed only in the sporophytic these cells in vascular plants. However, the path by which plants with these cells have evolved from generation of vascular plants. Therefore, it re- their nonvascular ancestors is unclear. We investigated genes of the moss Physcomitrella patens that mains unclear whether hydroids and stereids share encode NAC proteins. Loss-of-function mutants formed abnormal water-conducting and supporting an evolutionary lineage with xylem vessels and cells, as well as malformed sporophyte cells, and overexpression induced ectopic differentiation of fiber cells, respectively. water-conducting–like cells. Our results show conservation oftranscriptionalregulationandcellular The moss P. patens genome has eight loci that function between moss and Arabidopsis thaliana water-conducting cells. Theconservedgeneticbasis share similarity with VND/NST/SND (19–21). We suggests roles for NAC proteins in the adaptation of plants to land. sequenced cDNA from these genes and named the gene family PpVNS [VND-, NST/SND-, SMB he acquisition of water-conducting tis- transcriptional regulatory system for secondary (SOMBRERO)-related protein], with genes 1 through sue enabled the transition of plants from wall biosynthesis has been proposed (11). 8(22)(fig.S1andtableS1).Forphylogeneticanal- Tan aqueous environment to land. To achieve In mosses, specialized cell types have been ysis, publicly available genomic and transcriptomic this, vascular plants developed xylem vessel characterized. For example, hydroid cells conduct sequence data were searched. Although we iden- elements, cells that have a characteristic thick- water internally (12, 13), and mature hydroids tified a single gene of Marchantia polymorpha, ened secondary cell wall and undergo programmed cell death at maturity. These cells provide me- chanical strength to the stem, while allowing ef- REPORTS on February 27, 2015 ficient water conduction. Recent work revealed share several characteristics with xylem vessels Contribution of NAC Transcription from vascular plants, such as an elongated shape that a group of NAC [no apical meristem and an absence of cellular contents (13). How- ever, unlike xylem vessels, hydroids lack distinct Factors to Plant Adaptation to Land pits on their lateral walls, and there is an absence (NAM), Arabidopsis transcription activation factor of lignified secondary wall (14–17). Stereid cells Bo Xu,1 Misato Ohtani,2* Masatoshi Yamaguchi,1† Kiminori Toyooka,2 Mayumi Wakazaki,2 have thickened cell walls and are hypothesized to Mayuko Sato,2 Minoru Kubo,3‡ Yoshimi Nakano,1 Ryosuke Sano,1 Yuji Hiwatashi,3§ function as supporting elements (18). Both hydroids (ATAF1/2), and cup-shaped cotyledonTakashi Murata,3 (CUC)]Tetsuya Kurata,1 Arata Yoneda,1 Ko Kato,1 Mitsuyasu Hasebe,REPORTS3,4 Taku Demura1,2* and stereids are formed mainly in the gameto- The development of cells specialized for water conduction or support is a striking innovation of plants phytic generation, unlike xylem vessels and fiber transcription factors, includingthat VASCULAR- has enabled them to colonize land. The NAC transcription factors regulate the differentiationP. patens of ,cells,Selaginella which are formed moellendorffii only in the sporophytic, A. thaliana, plants (20, 21). We examined the tissue-specific ex- in tissues from protonemata and gametophytes. these cells in vascular plants. However, the path by which plants with these cells have evolvedpoplar, from andgeneration rice all of vascularhad many plants. (fig.Therefore, S2), it re- suggesting pression patterns of PpVNS by quantitative reverse In the gametophytic generation, after haploid spore RELATED NAC-DOMAIN6 (VND6)their nonvascular and ancestors VND7 is unclear. We investigated genes of the moss Physcomitrella patens that mains unclear whether hydroids and stereids share encode NAC proteins. Loss-of-function mutants formed abnormal water-conducting and supportingan early expansionan evolutionary lineage of VNS with xylemgenes vessels in and prevascular transcription polymerase chain reaction (qRT-PCR) germination, P. patens forms filamentous cells called of Arabidopsis thaliana,regulatexylemvesselcells, as well as malformed sporophyte cells, and overexpression induced ectopic differentiation of fiber cells, respectively. water-conducting–like cells. Our results show conservation oftranscriptionalregulationandcellular The moss P. patens genome has eight loci that function between moss and Arabidopsis thaliana water-conducting cells. TheconservedgeneticbasisFig. 2. Defectsshare similarity in with midribVND/NST/SND development(19–21). We in the differentiation by inducing genessuggests for roles sec for NACondary proteins in the adaptation of plants to land. sequenced cDNA from these genes and named ppvns1 ppvns6the gene family ppvns7PpVNS [VNDmutant.-, NST/SND(-,ASMBto C)Trans- he acquisition of water-conducting tis- transcriptional regulatory system for secondary (SOMBRERO)-related protein], with genes 1 through cell wall biosynthesis and xylem vesselsue enabled–specific the transition of plants from wall biosynthesis has been proposedport (11). of Evans8(22)(fig.S1andtableS1).Forphylogeneticanal- Blue dye in the leaves of wild-type www.sciencemag.org Tan aqueous environment to land. To achieveVascular Plant Innovaons (con/nued): In mosses, specialized cell types(WT) have been plantsysis, (A) publicly andREPORTS available in ppvns1 genomic and ppvns6 transcriptomic ppvns7 line 8 programmed cell death (1–6). NACthis, vascular plants proteins developed xylem vessel characterized. For example, hydroid cells conduct sequence data were searched. Although we iden- elements, cells that have a characteristic thick- water internally (12, 13), and mature(B) hydroids and linetified a 35 single (C) geneP. afterpatens of Marchantia, 30Selaginella min polymorpha moellendorffii of incubation., , A. thaliana, plants (20, 21). We examined the tissue-specific ex- in tissues from protonemata and gametophytes. also regulate the development of fiberened secondary cells: cell wall and scle- undergo programmedA conserved GRN for water conduc/on and support cells Arrowheads indicatepoplar, positions and rice all where had many Evans(fig. S2), suggesting Blue pression patterns of PpVNS by quantitative reverse In the gametophytic generation, after haploid spore cell death at maturity. These cells provide me- an early expansion of VNS genes in prevascular transcription polymerase chain reaction (qRT-PCR) germination,REPORTSP. patens forms filamentous cells called chanical strength to the stem, while allowing ef- dye was transported from the base. (D to I)Typical on February 27, 2015 renchyma cells found in vascularficient plants, water conduction. which Recent work revealed images of transmissionFig. electron 2. Defects in microscopy midrib development trans- in the that a group of NAC [no apical meristem ppvns1 ppvns6 ppvns7 mutant. (A to C)Trans- share several characteristics with xylem vessels (NAM), Arabidopsis transcription activation factor verse sections of theport tip of [(D) Evans and Blue dye (G)], in the middle leaves of wild-type [(E) from vascular plants, such as an elongated shape are also characterized by a thickened secondaryContribution of NAC Transcription(WT) plants (A) and in ppvns1 ppvns6 ppvns7 line 8 (ATAF1/2), and cup-shaped cotyledon (CUC)] and (H)], and basal [(F) and ( I)] regions of leaves of and an absence of cellular contents (13). How- transcription factors, including VASCULAR- (B) and line 35 (C) after 30 min of incubation. Arrowheads indicate positions where Evans Blue wall (7–10). In A. thaliana,NACSECONDARYRELATED NAC-DOMAIN6 (VND6) and VND7 wild-type plants [(D) to (F)] and ppvns1 ppvns6 ever, unlike xylem vessels, hydroids lack distinct Factors to Plant Adaptationdye was transported to from theLand base. (D to I)Typical of Arabidopsis thaliana,regulatexylemvessel ppvns7 [(G) to (I)]. h,images e, and of transmission s indicate electron content-free microscopy trans- pits on their lateral walls, and there is an absence differentiation by inducing genes for secondary WALL THICKENING PROMOTING FACTOR 1 2 1 verse sections of2 the tip [(D) and (G)], middle2 [(E) of lignified secondary wall (14–17). Stereid cells cell wall biosynthesis and xylem vesselBo–specific Xu, Misato Ohtani, * Masatoshihydroid Yamaguchi, cells† withKiminori thin Toyooka, cell walls,Mayumi epidermal Wakazaki, cells and (H)], and basal [(F) and ( I)] regions ofwww.sciencemag.org leaves of have
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