The soft glumes of common wheat are sterile-lemmas as determined by the domestication gene Q
|
摘要
The Q gene in common wheat encodes an APETALA2(AP2) transcription factor that causes the free threshing attribute. Wheat spikelets bearing several florets are subtended by a pair of soft glumes that allow free liberation of seeds. In wild species, the glumes are tough and rigid,making threshing difficult. However, the nature of these "soft glumes", caused by the domestication allele Q is not clear. Here, we found that over expression of Q in common wheat leads to homeotic florets at glume positions. We provide phenotypic, microscopy, and marker genes evidence to demonstrate that the soft glumes of common wheat are in fact lemma-like organs, or so-called sterile-lemmas. By comparing the structures subtending spikelets in wheat and other crops such as rice and maize, we found that AP2 genes may play conserved functions in grasses by manipulating vestigial structures, such as floret-derived soft glumes in wheat and empty glumes in rice. Conversion of these seemingly vegetative organs to reproductive organs may be useful in yield improvement of crop species.
The Q gene in common wheat encodes an APETALA2(AP2) transcription factor that causes the free threshing attribute. Wheat spikelets bearing several florets are subtended by a pair of soft glumes that allow free liberation of seeds. In wild species, the glumes are tough and rigid,making threshing difficult. However, the nature of these "soft glumes", caused by the domestication allele Q is not clear. Here, we found that over expression of Q in common wheat leads to homeotic florets at glume positions. We provide phenotypic, microscopy, and marker genes evidence to demonstrate that the soft glumes of common wheat are in fact lemma-like organs, or so-called sterile-lemmas. By comparing the structures subtending spikelets in wheat and other crops such as rice and maize, we found that AP2 genes may play conserved functions in grasses by manipulating vestigial structures, such as floret-derived soft glumes in wheat and empty glumes in rice. Conversion of these seemingly vegetative organs to reproductive organs may be useful in yield improvement of crop species.
The Q gene in common wheat encodes an APETALA2(AP2) transcription factor that causes the free threshing attribute. Wheat spikelets bearing several florets are subtended by a pair of soft glumes that allow free liberation of seeds. In wild species, the glumes are tough and rigid,making threshing difficult. However, the nature of these "soft glumes", caused by the domestication allele Q is not clear. Here, we found that over expression of Q in common wheat leads to homeotic florets at glume positions. We provide phenotypic, microscopy, and marker genes evidence to demonstrate that the soft glumes of common wheat are in fact lemma-like organs, or so-called sterile-lemmas. By comparing the structures subtending spikelets in wheat and other crops such as rice and maize, we found that AP2 genes may play conserved functions in grasses by manipulating vestigial structures, such as floret-derived soft glumes in wheat and empty glumes in rice. Conversion of these seemingly vegetative organs to reproductive organs may be useful in yield improvement of crop species.
引文
[1]J.Unrau,W.E.Smith,R.C.McGinnis,Spike density,speltoidy,and compactoidy in hexaploid wheat,Can.J.Res.28(1950)273-276.
[2]E.R.Sears,Misdivision of univalents in common wheat,Chromosoma 4(1952)535-550.
[3]E.R.Sears,The aneuploids of common wheat,Research Bulletin of Missouri Agricultural Experimental Station,572,1954,pp.1-59.
[4]J.MacKey,Neutron and X-ray experiments in wheat and a revision of the speltoid problem,Hereditas 40(1954)65-180.
[5]M.Muramatsu,Dosage effect of the spelta gene Q of hexaploid wheat,Genetics 48(1963)469-482.
[6]M.Muramatsu,Presence of Vulgare Gene,Q,in a Dense-spike Variety of Triticum dicoccum Schubl,Report of the Plant Germplasm Institute,4,Kyoto University,1979 39-41.
[7]M.Muramatsu,Spike type in two cultivars of Triticum dicoccum with the spelta gene q compared with the Q-bearing variety liguliforme,Jpn.J.Breed.35(1985)255-267.
[8]M.Muramatsu,The vulgare super gene,Q:its universality in durum wheat and its phenotypic effects in tetraploid and hexaploid wheats,Genome 28(1986)30-41.
[9]K.J.Simons,J.P.Fellers,H.N.Trick,Z.C.Zhang,Y.S.Tai,B.S.Gill,J.D.Faris,Molecular characterization of the major wheat domestication gene Q,Genetics 172(2006)547-555.
[10]K.D.Jofuku,B.G.den Boer,M.Van Montagu,J.K.Okamuro,Control of Arabidopsis flower and seed development by the homeotic gene APETALA2,Plant Cell 6(1994)1211-1225.
[11]M.Koornneef,J.H.de Bruine,P.Goettsch,A provisional map of chromosome 4 of Arabidopsis,Arabidopsis Inf.Serv.17(1980)11-18.
[12]G.Chuck,R.B.Meeley,S.Hake,The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1,Genes Dev.12(1998)1145-1154.
[13]D.Y.Lee,G.An,Two AP2 family genes,supernumerary bract(SNB)and Osindeterminate spikelet 1(OsIDS1),synergistically control inflorescence architecture and floral meristem establishment in rice,Plant J.69(2012)445-461.
[14]T.Nakano,K.Suzuki,T.Fujimura,H.Shinshi,Genome-wide analysis of the ERF gene family in Arabidopsis and rice,Plant Physiol.140(2006)411-432.
[15]B.Guo,Y.Wei,R.Xu,S.Lin,H.Luan,C.Lv,X.Zhang,X.Song,Genome-wide analysis of APETALA2/ethylene-responsive factor(AP2/ERF)gene family in barley(Hordeum vulgare L.),PLoS One 11(2016),e0161322.
[16]G.Chuck,R.Meeley,S.Hake,Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1and sid1,Development 135(2008)3013-3019.
[17]Z.Zhang,H.Belcram,P.Gornicki,M.Charles,J.Just,C.Huneau,G.Magdelenat,A.Couloux,S.Samain,B.S.Gill,J.B.Rasmussen,V.Barbe,J.D.Faris,B.Chalhoub,Duplication and partitioning in evolution and function of homoeologous Qloci governing domestication characters in polyploid wheat,Proc.Natl.Acad.Sci.U.S.A.108(2011)18737-18742.
[18]J.M.Debernardi,H.Lin,G.Chuck,J.D.Faris,J.Dubcovsky,microRNA172 plays a crucial role in wheat spike morphogenesis and grain threshability,Development 144(2017)1966-1975.
[19]J.R.Greenwood,E.J.Finnegan,N.Watanabe,B.Trevaskis,S.M.Swain,New alleles of the wheat domestication gene Q reveal multiple roles in growth and reproductive development,Development 144(2017)1959-1965.
[20]X.C.Gao,W.Q.Liang,C.S.Yin,S.M.Ji,H.M.Wang,X.A.Su,C.C.Guo,H.Z.Kong,H.W.Xue,D.B.Zhang,The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development,Plant Physiol.153(2010)728-740.
[21]I.Khanday,S.R.Yadav,U.Vijayraghavan,Rice LHS1/OsMADS1controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways,Plant Physiol.161(2013)1970-1983.
[22]X.Lin,F.Wu,X.Du,X.Shi,Y.Liu,S.Liu,Y.Hu,G.Theissen,Z.Meng,The pleiotropic SEPALLATA-like gene OsMADS34reveals that the'empty glumes'of rice(Oryza sativa)spikelets are in fact rudimentary lemmas,New Phytol.202(2014)689-702.
[23]G.Agrawal,K.Abe,M.Yamazaki,A.Miyao,H.Hirochika,Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-offunction mutants of the OsMADS1 gene,Plant Mol.Biol.59(2005)125-135.
[24]R.F.Cui,J.K.Han,S.Z.Zhao,K.M.Su,F.Wu,X.Q.Du,Q.J.Xu,K.Chong,G.Theissen,Z.Meng,Functional conservation and diversification of class E floral homeotic genes in rice(Oryza sativa),Plant J.61(2010)767-781.
[25]K.Murai,Homeotic genes and the ABCDE model for floral organ formation in wheat,Plants 2(2013)379-395.
[26]D.Y.Lee,J.Lee,S.Moon,S.Y.Park,G.An,The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem,Plant J.49(2007)64-78.
[27]D.Y.Ren,Y.F.Li,F.M.Zhao,X.C.Sang,J.Q.Shi,N.Wang,S.Guo,Y.H.Ling,C.W.Zhang,Z.L.Yang,G.H.He,MULTI-FLORETSPIKELET1,which encodes an AP2/ERF protein,determines spikelet meristem fate and sterile lemma identity in rice,Plant Physiol.162(2013)872-884.
[28]K.J.Zhao,J.Xiao,Y.Liu,S.L.Chen,C.X.Yuan,A.Z.Cao,F.M.You,D.L.Yang,S.M.An,H.Y.Wang,X.E.Wang,Rht23(5Dq′)likely encodes a Q homeologue with pleiotropic effects on plant height and spike compactness,Theor.Appl.Genet.131(2018)1825-1834.
[29]J.D.Fairs,Q.J.Zhang,S.M.Chao,Z.C.Zhang,S.S.Xu,Analysis of agronomic and domestication traits in a durum×cultivated emmer wheat population using a high-density single nucleotide polymorphism-based linkage map,Theor.Appl.Genet.127(2014)2333-2348.
[30]T.Zhang,Y.Li,L.Ma,X.Sang,Y.Ling,Y.Wang,P.Yu,H.Zhuang,J.Huang,N.Wang,F.Zhao,C.Zhang,Z.Yang,L.Fang,G.He,LATERAL FLORET 1 induced the three-florets spikelet in rice,Proc.Natl.Acad.Sci.U.S.A.114(2017)9984-9989.
[2]E.R.Sears,Misdivision of univalents in common wheat,Chromosoma 4(1952)535-550.
[3]E.R.Sears,The aneuploids of common wheat,Research Bulletin of Missouri Agricultural Experimental Station,572,1954,pp.1-59.
[4]J.MacKey,Neutron and X-ray experiments in wheat and a revision of the speltoid problem,Hereditas 40(1954)65-180.
[5]M.Muramatsu,Dosage effect of the spelta gene Q of hexaploid wheat,Genetics 48(1963)469-482.
[6]M.Muramatsu,Presence of Vulgare Gene,Q,in a Dense-spike Variety of Triticum dicoccum Schubl,Report of the Plant Germplasm Institute,4,Kyoto University,1979 39-41.
[7]M.Muramatsu,Spike type in two cultivars of Triticum dicoccum with the spelta gene q compared with the Q-bearing variety liguliforme,Jpn.J.Breed.35(1985)255-267.
[8]M.Muramatsu,The vulgare super gene,Q:its universality in durum wheat and its phenotypic effects in tetraploid and hexaploid wheats,Genome 28(1986)30-41.
[9]K.J.Simons,J.P.Fellers,H.N.Trick,Z.C.Zhang,Y.S.Tai,B.S.Gill,J.D.Faris,Molecular characterization of the major wheat domestication gene Q,Genetics 172(2006)547-555.
[10]K.D.Jofuku,B.G.den Boer,M.Van Montagu,J.K.Okamuro,Control of Arabidopsis flower and seed development by the homeotic gene APETALA2,Plant Cell 6(1994)1211-1225.
[11]M.Koornneef,J.H.de Bruine,P.Goettsch,A provisional map of chromosome 4 of Arabidopsis,Arabidopsis Inf.Serv.17(1980)11-18.
[12]G.Chuck,R.B.Meeley,S.Hake,The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1,Genes Dev.12(1998)1145-1154.
[13]D.Y.Lee,G.An,Two AP2 family genes,supernumerary bract(SNB)and Osindeterminate spikelet 1(OsIDS1),synergistically control inflorescence architecture and floral meristem establishment in rice,Plant J.69(2012)445-461.
[14]T.Nakano,K.Suzuki,T.Fujimura,H.Shinshi,Genome-wide analysis of the ERF gene family in Arabidopsis and rice,Plant Physiol.140(2006)411-432.
[15]B.Guo,Y.Wei,R.Xu,S.Lin,H.Luan,C.Lv,X.Zhang,X.Song,Genome-wide analysis of APETALA2/ethylene-responsive factor(AP2/ERF)gene family in barley(Hordeum vulgare L.),PLoS One 11(2016),e0161322.
[16]G.Chuck,R.Meeley,S.Hake,Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1and sid1,Development 135(2008)3013-3019.
[17]Z.Zhang,H.Belcram,P.Gornicki,M.Charles,J.Just,C.Huneau,G.Magdelenat,A.Couloux,S.Samain,B.S.Gill,J.B.Rasmussen,V.Barbe,J.D.Faris,B.Chalhoub,Duplication and partitioning in evolution and function of homoeologous Qloci governing domestication characters in polyploid wheat,Proc.Natl.Acad.Sci.U.S.A.108(2011)18737-18742.
[18]J.M.Debernardi,H.Lin,G.Chuck,J.D.Faris,J.Dubcovsky,microRNA172 plays a crucial role in wheat spike morphogenesis and grain threshability,Development 144(2017)1966-1975.
[19]J.R.Greenwood,E.J.Finnegan,N.Watanabe,B.Trevaskis,S.M.Swain,New alleles of the wheat domestication gene Q reveal multiple roles in growth and reproductive development,Development 144(2017)1959-1965.
[20]X.C.Gao,W.Q.Liang,C.S.Yin,S.M.Ji,H.M.Wang,X.A.Su,C.C.Guo,H.Z.Kong,H.W.Xue,D.B.Zhang,The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development,Plant Physiol.153(2010)728-740.
[21]I.Khanday,S.R.Yadav,U.Vijayraghavan,Rice LHS1/OsMADS1controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways,Plant Physiol.161(2013)1970-1983.
[22]X.Lin,F.Wu,X.Du,X.Shi,Y.Liu,S.Liu,Y.Hu,G.Theissen,Z.Meng,The pleiotropic SEPALLATA-like gene OsMADS34reveals that the'empty glumes'of rice(Oryza sativa)spikelets are in fact rudimentary lemmas,New Phytol.202(2014)689-702.
[23]G.Agrawal,K.Abe,M.Yamazaki,A.Miyao,H.Hirochika,Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-offunction mutants of the OsMADS1 gene,Plant Mol.Biol.59(2005)125-135.
[24]R.F.Cui,J.K.Han,S.Z.Zhao,K.M.Su,F.Wu,X.Q.Du,Q.J.Xu,K.Chong,G.Theissen,Z.Meng,Functional conservation and diversification of class E floral homeotic genes in rice(Oryza sativa),Plant J.61(2010)767-781.
[25]K.Murai,Homeotic genes and the ABCDE model for floral organ formation in wheat,Plants 2(2013)379-395.
[26]D.Y.Lee,J.Lee,S.Moon,S.Y.Park,G.An,The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem,Plant J.49(2007)64-78.
[27]D.Y.Ren,Y.F.Li,F.M.Zhao,X.C.Sang,J.Q.Shi,N.Wang,S.Guo,Y.H.Ling,C.W.Zhang,Z.L.Yang,G.H.He,MULTI-FLORETSPIKELET1,which encodes an AP2/ERF protein,determines spikelet meristem fate and sterile lemma identity in rice,Plant Physiol.162(2013)872-884.
[28]K.J.Zhao,J.Xiao,Y.Liu,S.L.Chen,C.X.Yuan,A.Z.Cao,F.M.You,D.L.Yang,S.M.An,H.Y.Wang,X.E.Wang,Rht23(5Dq′)likely encodes a Q homeologue with pleiotropic effects on plant height and spike compactness,Theor.Appl.Genet.131(2018)1825-1834.
[29]J.D.Fairs,Q.J.Zhang,S.M.Chao,Z.C.Zhang,S.S.Xu,Analysis of agronomic and domestication traits in a durum×cultivated emmer wheat population using a high-density single nucleotide polymorphism-based linkage map,Theor.Appl.Genet.127(2014)2333-2348.
[30]T.Zhang,Y.Li,L.Ma,X.Sang,Y.Ling,Y.Wang,P.Yu,H.Zhuang,J.Huang,N.Wang,F.Zhao,C.Zhang,Z.Yang,L.Fang,G.He,LATERAL FLORET 1 induced the three-florets spikelet in rice,Proc.Natl.Acad.Sci.U.S.A.114(2017)9984-9989.