Identification and characterization of cell cultures with various embryogenic/regenerative potential in cotton based on morphological,cytochemical,and cytogenetical assessment
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摘要
Somatic embryogenesis(SE) plays a vital role in genetic transformation and massive propagation of important agronomical and economical crops.Here,we conducted a systematic assessment of the morphological,cytochemical,and cytogenetical characteristics of six culture strains with various embryogenic/regenerative potential during SE process in cotton.Results indicated that the six cell culture strains had stable ploidy levels,and did not reveal any relationship between the cytogenetic state and their morphogenetic potential.Moreover,the six culture strains were compared via double staining with Evans blue and Acetocarmine to efficiently distinguish embryogenic and non-embryogenic cells and determine the embryogenic nature of the calli.In addition,the kind of auxins added in medium affected not only growth property,color,size of cell clumps but also ploidy level and regeneration ability.By combining analysis of morphological,cytochemical,and cytogenetical characteristics of the cell cultures,we are able to obtain and maintain homogeneous cell population with high morphogenic and regeneration ability and establish efficient somatic embryogenesis and regeneration system from short-term cell cultures in upland cotton,which highlight the application of biotechnological approaches in crop breeding,and above all,to better understand totipotency of cells in higher plants.
Somatic embryogenesis(SE) plays a vital role in genetic transformation and massive propagation of important agronomical and economical crops.Here,we conducted a systematic assessment of the morphological,cytochemical,and cytogenetical characteristics of six culture strains with various embryogenic/regenerative potential during SE process in cotton.Results indicated that the six cell culture strains had stable ploidy levels,and did not reveal any relationship between the cytogenetic state and their morphogenetic potential.Moreover,the six culture strains were compared via double staining with Evans blue and Acetocarmine to efficiently distinguish embryogenic and non-embryogenic cells and determine the embryogenic nature of the calli.In addition,the kind of auxins added in medium affected not only growth property,color,size of cell clumps but also ploidy level and regeneration ability.By combining analysis of morphological,cytochemical,and cytogenetical characteristics of the cell cultures,we are able to obtain and maintain homogeneous cell population with high morphogenic and regeneration ability and establish efficient somatic embryogenesis and regeneration system from short-term cell cultures in upland cotton,which highlight the application of biotechnological approaches in crop breeding,and above all,to better understand totipotency of cells in higher plants.
Somatic embryogenesis(SE) plays a vital role in genetic transformation and massive propagation of important agronomical and economical crops.Here,we conducted a systematic assessment of the morphological,cytochemical,and cytogenetical characteristics of six culture strains with various embryogenic/regenerative potential during SE process in cotton.Results indicated that the six cell culture strains had stable ploidy levels,and did not reveal any relationship between the cytogenetic state and their morphogenetic potential.Moreover,the six culture strains were compared via double staining with Evans blue and Acetocarmine to efficiently distinguish embryogenic and non-embryogenic cells and determine the embryogenic nature of the calli.In addition,the kind of auxins added in medium affected not only growth property,color,size of cell clumps but also ploidy level and regeneration ability.By combining analysis of morphological,cytochemical,and cytogenetical characteristics of the cell cultures,we are able to obtain and maintain homogeneous cell population with high morphogenic and regeneration ability and establish efficient somatic embryogenesis and regeneration system from short-term cell cultures in upland cotton,which highlight the application of biotechnological approaches in crop breeding,and above all,to better understand totipotency of cells in higher plants.
引文
Bhargava A,Osusky M,Forward B S,Hancock R E,Kay WW,Misra S.2007.Expression of a polyphemusin variant in transgenic tobacco confers resistance against plant pathogenic bacteria,fungi and a virus.Plant Cell Tissue and Organ Culture,88,301-312.
Brada?F,Pliego-Alfaro F,Sánchez-Romero C.2016.Somaclonal variation in olive(Olea europaea L.)plants regenerated via somatic embryogenesis:Influence of genotype and culture age on phenotypic stability.Scientia Horticulturae,213,208-215.
Egertsdotter U,Arnold S V.1998.Development of somatic embryos in Norway spruce.Journal of Experimental Botany,49,155-162.
Filonova L H,Bozhkov P V,Arnold S V.2000.Developmental pathway of somatic embryogenesis in Picea abies as revealed by time-lapse tracking.Journal of Experimental Botany,51,249-264.
Gomes H T,Bartos P M C,Scherwinski-Pereira J E.2017.Dynamics of morphological and anatomical changes in leaf tissues of an interspecific hybrid of oil palm during acquisition and development of somatic embryogenesis.Plant Cell Tissue and Organ Culture,131,269-282.
Gupta P K,Durzan D J.1987.Biotechnology of somatic polyembryogenesis and plantlet regeneration in loblolly pine.Nature Biotechnology,5,147-151.
Ikeuchi M,Sugimoto K,Iwase A.2013.Plant callus:Mechanisms of induction and repression.The Plant Cell,25,3159-3173.
Jiménez V M.2005.Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis.Plant Growth Regulation,47,91-110.
Kennedy D,Norman C.2005.What don’t we know?Science,309,75.
Kim H J,Triplett B A.2001.Cotton fiber growth in planta and in vitro.Models for plant cell elongation and cell wall biogenesis.Journal of Plant Physiology,127,1361-1366.
Kuo L Y,Huang Y J,Chang J,Chiou W L,Huang Y M.2017.Evaluating the spore genome sizes of ferns and lycophytes:A flow cytometry approach.New Phytologist,213,1974-1983.
Landey R B,Cenci A,Guyot R,Bertrand B,Georget F,Dechamp E,Herrera J C,Aribi J,Lashermes P,Etienne H.2015.Assessment of genetic and epigenetic changes during cell culture ageing and relations with somaclonal variation in Coffea arabica.Plant Cell Tissue and Organ Culture,122,517-531.
Lelu-Walter M A,Thompson D,Harvengt L,Sanchez L,Toribio M,Paques L E.2013.Somatic embryogenesis in forestry with a focus on Europe:State-of-the-art,benefits,challenges and future direction.Tree Genetics&Genomes,9,883-899.
Loyolavargas V M,Delape?a C,Galazávalos R M,Quirozfigueroa F R.2008.Plant tissue culture.In:Walker J,Rapley R,eds.,Molecular Biomethods Handbook.Humana Press,Totowa.pp.875-904.
Minina E A,Filonova L H,Daniel G,Bozhkov P V.2013.Detection and measurement of necrosis in plants.In:McCall K,Klein C,eds.,Methods in Molecular Biology.Humana Press,Totowa.pp.229-248.
Mohajer S,Taha R M,Khorasani A,Yaacob J S.2012.Induction of different types of callus and somatic embryogenesis in various explants of Sainfoin(Onobrychis sativa).Australian Journal of Crop Science,6,1305-1313.
Moradi Z,Farahani F,Sheidai M,Satari T N.2017.Somaclonal variation in banana(Musa acuminate colla cv.Valery)regenerated plantlets from somatic embryogenesis:Histological and cytogenetic approaches.Caryologia,70,1-6.
Pádua M S,Paiva L V,Silva L C D,Livramento K G D,Alves E,Castro A H F.2014.Morphological characteristics and cell viability of coffee plants calli.Rural Science,44,660-665.
Pellicer J,Leitch I J.2014.The application of flow cytometry for estimating genome size and ploidy level in plants.In:Besse P,ed.,Molecular Plant Taxonomy.Humana Press,Totowa.pp.279-307.
Qin Y M,Zhu Y X.2011.How cotton fibers elongate:A tale of linear cell-growth mode.Current Opinion in Plant Biology,14,106-111.
Ruan Y L,Llewellyn D J,Furbank R T.2003.Suppression of sucrose synthase gene expression represses cotton fiber cell initiation,elongation,and seed development.The Plant Cell,15,952-964.
Sakhanokho H F,Rajasekaran K.2016.Cotton regeneration in vitro.In:Ramawat K G,Ahuja M R,eds.,Fiber Plants.Springer,Cham.pp.87-110.
San JoséM D C,Corredoira E,Oliveira H,Santos C.2015.Cryopreservation of somatic embryos of Alnus glutinosa(L.)Gaertn.and confirmation of ploidy stability by flow cytometry.Plant Cell Tissue and Organ Culture,123,489-499.
Santos A L W D,Silveira V,Steiner N,Vidor M,Guerra M P.2002.Somatic embryogenesis in parana pine(Araucaria angustifolia(Bert.)O.Kuntze).Brazilian Archives of Biology and Technology,45,97-106.
Santos D N D,Nunes C F,Soares J D R,Alves E,Labory C R G,Pasqual M,Pio L A S.2015.Ultrastructural and cytochemical analysis of physic nut callus tissue in response to different combinations of growth regulators.Acta Scientiarum-Agronomy,37,355-359.
Steiner N,Farias-Soares F L,SchmidtéC,Pereira M L,Scheid B,Rogge-Renner G D,Bouzon Z L,Schmidt D,Maldonado S,Guerra M P.2016.Toward establishing a morphological and ultrastructural characterization of proembryogenic masses and early somatic embryos of Araucaria angustifolia(Bert.)O.Kuntze.Protoplasma,253,487-501.
Steiner N,Vieira F D N,Maldonado S,Guerra M P.2005.Effect of carbon source on morphology and histodifferentiation of Araucaria angustifolia embryogenic cultures.Brazilian Archives of Biology and Technology,48,895-903.
Suarez M F,Filonova L H,Smertenko A,Savenkov E I,Clapham D H,Arnold S,Zhivotovsky B,Bozhkov P V.2004.Metacaspase-dependent programmed cell death is essential for plant embryogenesis.Current Biology,14,339-340.
Sun Y,Zhang X,Nie Y,Guo X,Jin S,Liang S.2004.Production and characterization of somatic hybrids between upland cotton(Gossypium hirsutum)and wild cotton(G.klotzschianum Anderss)via electrofusion.Theoretical and Applied Genetics,109,472-479.
Vogel G.2005.How does a single somatic cell become a whole plant?Science,309,86.
Wilkins T A,Rajasekaran K,Anderson D M.2000.Cotton biotechnology.Critical Reviews in Plant Sciences,19,511-550.
Wilkins T A,Mishra R,Trolinder N L.2004.Agrobacteriummediated transformation and regeneration of cotton.Journal of Food Agriculture and Environment,2,179-187.
Wu J,Zhang X,Nie Y,Jin S,Liang S.2004.Factors affecting somatic embryogenesis and plant regeneration from a range of recalcitrant genotypes of Chinese cottons(Gossypium hirsutum L.).In Vitro Cellular&Developmental BiologyPlant,40,371-375.
Xu K,Chang Y,Liu K,Wang F,Liu Z Y,Zhang T,Li T G,Zhang Y,Zhang F,Zhang J,Wang Y,Niu W,Jia S,Xie H,Tan G,Li C.2015.Regeneration of Solanum nigrum by somatic embryogenesis,involving frog egg-like body,a novel structure.PLoS ONE,10,e0125645.
Yan J,Zhang J,Sun K,Chang D,Bai S,Shen Y,Huang L,Zhang J,Zhang Y,Dong Y.2016.Ploidy level and DNAcontent of Erianthus arundinaceus as determined by flow cytometry and the association with biological characteristics.PLoS ONE,11,e0151948.
Zeng F,Zhang X,Jin S,Cheng L,Liang S,Hu L,Guo X,Nie Y,Cao J.2007.Chromatin reorganization and endogenous auxin/cytokinin dynamic activity during somatic embryogenesis of cultured cotton cell.Plant Cell Tissue and Organ Culture,90,63-70.
Zeng F,Zhang X,Zhu L,Tu L,Guo X,Nie Y.2006.Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray.Plant Molecular Biology,60,167-183.
Zhang T,Qian N,Zhu X,Chen H,Wang S,Mei H,Zhang Y.2013.Variations and transmission of QTL alleles for yield and fiber qualities in upland cotton cultivars developed in China.PLoS ONE,8,e57220.
Zimmerman J L.1993.Somatic embryogenesis:a model for early development in higher plants.The Plant Cell,5,1411-1423.
Brada?F,Pliego-Alfaro F,Sánchez-Romero C.2016.Somaclonal variation in olive(Olea europaea L.)plants regenerated via somatic embryogenesis:Influence of genotype and culture age on phenotypic stability.Scientia Horticulturae,213,208-215.
Egertsdotter U,Arnold S V.1998.Development of somatic embryos in Norway spruce.Journal of Experimental Botany,49,155-162.
Filonova L H,Bozhkov P V,Arnold S V.2000.Developmental pathway of somatic embryogenesis in Picea abies as revealed by time-lapse tracking.Journal of Experimental Botany,51,249-264.
Gomes H T,Bartos P M C,Scherwinski-Pereira J E.2017.Dynamics of morphological and anatomical changes in leaf tissues of an interspecific hybrid of oil palm during acquisition and development of somatic embryogenesis.Plant Cell Tissue and Organ Culture,131,269-282.
Gupta P K,Durzan D J.1987.Biotechnology of somatic polyembryogenesis and plantlet regeneration in loblolly pine.Nature Biotechnology,5,147-151.
Ikeuchi M,Sugimoto K,Iwase A.2013.Plant callus:Mechanisms of induction and repression.The Plant Cell,25,3159-3173.
Jiménez V M.2005.Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis.Plant Growth Regulation,47,91-110.
Kennedy D,Norman C.2005.What don’t we know?Science,309,75.
Kim H J,Triplett B A.2001.Cotton fiber growth in planta and in vitro.Models for plant cell elongation and cell wall biogenesis.Journal of Plant Physiology,127,1361-1366.
Kuo L Y,Huang Y J,Chang J,Chiou W L,Huang Y M.2017.Evaluating the spore genome sizes of ferns and lycophytes:A flow cytometry approach.New Phytologist,213,1974-1983.
Landey R B,Cenci A,Guyot R,Bertrand B,Georget F,Dechamp E,Herrera J C,Aribi J,Lashermes P,Etienne H.2015.Assessment of genetic and epigenetic changes during cell culture ageing and relations with somaclonal variation in Coffea arabica.Plant Cell Tissue and Organ Culture,122,517-531.
Lelu-Walter M A,Thompson D,Harvengt L,Sanchez L,Toribio M,Paques L E.2013.Somatic embryogenesis in forestry with a focus on Europe:State-of-the-art,benefits,challenges and future direction.Tree Genetics&Genomes,9,883-899.
Loyolavargas V M,Delape?a C,Galazávalos R M,Quirozfigueroa F R.2008.Plant tissue culture.In:Walker J,Rapley R,eds.,Molecular Biomethods Handbook.Humana Press,Totowa.pp.875-904.
Minina E A,Filonova L H,Daniel G,Bozhkov P V.2013.Detection and measurement of necrosis in plants.In:McCall K,Klein C,eds.,Methods in Molecular Biology.Humana Press,Totowa.pp.229-248.
Mohajer S,Taha R M,Khorasani A,Yaacob J S.2012.Induction of different types of callus and somatic embryogenesis in various explants of Sainfoin(Onobrychis sativa).Australian Journal of Crop Science,6,1305-1313.
Moradi Z,Farahani F,Sheidai M,Satari T N.2017.Somaclonal variation in banana(Musa acuminate colla cv.Valery)regenerated plantlets from somatic embryogenesis:Histological and cytogenetic approaches.Caryologia,70,1-6.
Pádua M S,Paiva L V,Silva L C D,Livramento K G D,Alves E,Castro A H F.2014.Morphological characteristics and cell viability of coffee plants calli.Rural Science,44,660-665.
Pellicer J,Leitch I J.2014.The application of flow cytometry for estimating genome size and ploidy level in plants.In:Besse P,ed.,Molecular Plant Taxonomy.Humana Press,Totowa.pp.279-307.
Qin Y M,Zhu Y X.2011.How cotton fibers elongate:A tale of linear cell-growth mode.Current Opinion in Plant Biology,14,106-111.
Ruan Y L,Llewellyn D J,Furbank R T.2003.Suppression of sucrose synthase gene expression represses cotton fiber cell initiation,elongation,and seed development.The Plant Cell,15,952-964.
Sakhanokho H F,Rajasekaran K.2016.Cotton regeneration in vitro.In:Ramawat K G,Ahuja M R,eds.,Fiber Plants.Springer,Cham.pp.87-110.
San JoséM D C,Corredoira E,Oliveira H,Santos C.2015.Cryopreservation of somatic embryos of Alnus glutinosa(L.)Gaertn.and confirmation of ploidy stability by flow cytometry.Plant Cell Tissue and Organ Culture,123,489-499.
Santos A L W D,Silveira V,Steiner N,Vidor M,Guerra M P.2002.Somatic embryogenesis in parana pine(Araucaria angustifolia(Bert.)O.Kuntze).Brazilian Archives of Biology and Technology,45,97-106.
Santos D N D,Nunes C F,Soares J D R,Alves E,Labory C R G,Pasqual M,Pio L A S.2015.Ultrastructural and cytochemical analysis of physic nut callus tissue in response to different combinations of growth regulators.Acta Scientiarum-Agronomy,37,355-359.
Steiner N,Farias-Soares F L,SchmidtéC,Pereira M L,Scheid B,Rogge-Renner G D,Bouzon Z L,Schmidt D,Maldonado S,Guerra M P.2016.Toward establishing a morphological and ultrastructural characterization of proembryogenic masses and early somatic embryos of Araucaria angustifolia(Bert.)O.Kuntze.Protoplasma,253,487-501.
Steiner N,Vieira F D N,Maldonado S,Guerra M P.2005.Effect of carbon source on morphology and histodifferentiation of Araucaria angustifolia embryogenic cultures.Brazilian Archives of Biology and Technology,48,895-903.
Suarez M F,Filonova L H,Smertenko A,Savenkov E I,Clapham D H,Arnold S,Zhivotovsky B,Bozhkov P V.2004.Metacaspase-dependent programmed cell death is essential for plant embryogenesis.Current Biology,14,339-340.
Sun Y,Zhang X,Nie Y,Guo X,Jin S,Liang S.2004.Production and characterization of somatic hybrids between upland cotton(Gossypium hirsutum)and wild cotton(G.klotzschianum Anderss)via electrofusion.Theoretical and Applied Genetics,109,472-479.
Vogel G.2005.How does a single somatic cell become a whole plant?Science,309,86.
Wilkins T A,Rajasekaran K,Anderson D M.2000.Cotton biotechnology.Critical Reviews in Plant Sciences,19,511-550.
Wilkins T A,Mishra R,Trolinder N L.2004.Agrobacteriummediated transformation and regeneration of cotton.Journal of Food Agriculture and Environment,2,179-187.
Wu J,Zhang X,Nie Y,Jin S,Liang S.2004.Factors affecting somatic embryogenesis and plant regeneration from a range of recalcitrant genotypes of Chinese cottons(Gossypium hirsutum L.).In Vitro Cellular&Developmental BiologyPlant,40,371-375.
Xu K,Chang Y,Liu K,Wang F,Liu Z Y,Zhang T,Li T G,Zhang Y,Zhang F,Zhang J,Wang Y,Niu W,Jia S,Xie H,Tan G,Li C.2015.Regeneration of Solanum nigrum by somatic embryogenesis,involving frog egg-like body,a novel structure.PLoS ONE,10,e0125645.
Yan J,Zhang J,Sun K,Chang D,Bai S,Shen Y,Huang L,Zhang J,Zhang Y,Dong Y.2016.Ploidy level and DNAcontent of Erianthus arundinaceus as determined by flow cytometry and the association with biological characteristics.PLoS ONE,11,e0151948.
Zeng F,Zhang X,Jin S,Cheng L,Liang S,Hu L,Guo X,Nie Y,Cao J.2007.Chromatin reorganization and endogenous auxin/cytokinin dynamic activity during somatic embryogenesis of cultured cotton cell.Plant Cell Tissue and Organ Culture,90,63-70.
Zeng F,Zhang X,Zhu L,Tu L,Guo X,Nie Y.2006.Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray.Plant Molecular Biology,60,167-183.
Zhang T,Qian N,Zhu X,Chen H,Wang S,Mei H,Zhang Y.2013.Variations and transmission of QTL alleles for yield and fiber qualities in upland cotton cultivars developed in China.PLoS ONE,8,e57220.
Zimmerman J L.1993.Somatic embryogenesis:a model for early development in higher plants.The Plant Cell,5,1411-1423.