Sugar metabolism plays an essential role in plant male reproduction. Defects in sugar metabolism during anther and pollen development often result in genic male sterility(GMS). In this review, we summarize the recent ...Sugar metabolism plays an essential role in plant male reproduction. Defects in sugar metabolism during anther and pollen development often result in genic male sterility(GMS). In this review, we summarize the recent progresses of the sugar metabolism-related GMS genes and their roles during plant anther and pollen development, including callose wall and primexine formation, intine development, pollen maturation and starch accumulation, anther dehiscence, and pollen germination and tube growth. We predict 112 putative sugar metabolic GMS genes in maize based on bioinformatics and RNA-seq analyses, and most of them have peak expression patterns during middle or late anther developmental stages.Finally, we outline the potential applications of sugar metabolic GMS genes in crop hybrid breeding and seed production. This review will deepen our understanding on sugar metabolic pathways in controlling pollen development and male fertility in plants.展开更多
1.Introduction Global food security faces a severe challenge,as world population is predicted to grow by 25%and reach 10 billion by the mid-21 st century[1].With limited agricultural land and fresh water,greater and m...1.Introduction Global food security faces a severe challenge,as world population is predicted to grow by 25%and reach 10 billion by the mid-21 st century[1].With limited agricultural land and fresh water,greater and more sustainable crop production needs to be achieved by use of modern agricultural technologies[2,3].Among these are developing and exploiting more efficient heterosis utilization strategy with male sterile lines for hybrid breeding and seed production.展开更多
Because of its significance for plant male fertility and,hence,direct impact on crop yield,pollen exine development has inspired decades of scientific inquiry.However,the molecularmechanismunderlying exine formation a...Because of its significance for plant male fertility and,hence,direct impact on crop yield,pollen exine development has inspired decades of scientific inquiry.However,the molecularmechanismunderlying exine formation and thickness remains elusive.In this study,we identified that a previously unrecognized repressor,ZmMS1/ZmLBD30,controls proper pollen exine development in maize.Using an ms1 mutant with aberrantly thickened exine,we cloned a male-sterility gene,ZmMs1,which encodes a tapetum-specific lateral organ boundary domain transcription factor,ZmLBD30.Weshowed thatZmMs1/ZmLBD30 is initially turned on by a transcriptional activation cascade of ZmbHLH51-ZmMYB84-ZmMS7,and then it serves as a repressor to shut down this cascade via feedback repression to ensure timely tapetal degeneration and proper level of exine.This activation-feedback repression loop regulating male fertility is conserved in maize and sorghum,and similar regulatory mechanism may also exist in other flowering plants such as rice and Arabidopsis.Collectively,these findings reveal a novel regulatory mechanism of pollen exine development by which a long-sought master repressor of upstream activators prevents excessive exine formation.展开更多
Genic male sterility (GMS) is very useful for hybrid vigor utilization and hybrid seed production. Although a large number of GMS genes have been identified in plants, little is known about the roles of GDSL lipase me...Genic male sterility (GMS) is very useful for hybrid vigor utilization and hybrid seed production. Although a large number of GMS genes have been identified in plants, little is known about the roles of GDSL lipase members in anther and pollen development. Here, we report a maize GMS gene, ZmMs30, which encodes a novel type of GDSL lipase with diverged catalytic residues. Enzyme kinetics and activity assays show that ZmMs30 has lipase activity and prefers to substrates with a short carbon chain. ZmMs30 is specifically expressed in maize anthers during stages 7-9. Loss of ZmMs30 function resulted in defective anther cuticle, irregular foot layer of pollen exine, and complete male sterility. Cytological and lipidomics analyses demonstrate that ZmMs30 is crucial for the aliphatic metabolic pathway required for pollen exine formation and anther cuticle development. Furthermore, we found that male sterility caused by loss of ZmMs30 function was stable in various inbred lines with different genetic background, and that it didn't show any negative effect on maize heterosis and production, suggesting that ZmMs30 is valuable for crossbreeding and hybrid seed production. We then developed a new multi-control sterility system using ZmMs30 and its mutant line, and demonstrated it is feasible for generating desirable GMS lines and valu. able for hybrid maize seed production. Taken together, our study sheds new light on the mechanisms of anther and pollen development, and provides a valuable male-sterility system for hybrid breeding maize.展开更多
As one of the most important crops, maize not only has been a source of the food, feed, and industrial feedstock for biofuel and bioproducts, but also became a model plant system for addressing fundamental questions i...As one of the most important crops, maize not only has been a source of the food, feed, and industrial feedstock for biofuel and bioproducts, but also became a model plant system for addressing fundamental questions in genetics. Male sterility is a very useful trait for hybrid vigor utilization and hybrid seed production. The identification and characterization of genic male-sterility (GMS) genes in maize and other plants have deepened our understanding of the molecular mechanisms controlling anther and pollen development, and enabled the development and efficient use of many biotechnology-based male-sterility (BMS) systems for crop hybrid breeding. In this review, we summarize main advances on the identification and characterization of GMS genes in maize, and con struct a putative regulatory network controlling maize anther and pollen development by comparative genomic analysis of GMS genes in maize, Arabidopsis, and rice. Furthermore, we discuss and appraise the features of more than a dozen BMS systems for propagating male-sterile lines and producing hybrid seeds in maize and other plants. Finally, we provide our perspectives on the studies of GMS genes and the development of novel BMS systems in maize and other plants. The continuous exploration of GMS genes and BMS systems will enhance our understanding of molecular regulatory networks controlling male fertility and greatly facilitate hybrid vigor utilization in breeding and field production of maize and other crops.展开更多
Fatty acids and their derivatives are essential building blocks for anther cuticle and pollen wall formation.Disruption of lipid metabolism during anther and pollen development often leads to genic male sterility(GMS)...Fatty acids and their derivatives are essential building blocks for anther cuticle and pollen wall formation.Disruption of lipid metabolism during anther and pollen development often leads to genic male sterility(GMS).To date,many lipid metabolism-related GMS genes that are involved in the formation of anther cuticle,pollen wall,and subcellular organelle membranes in anther wall layers have been identified and characterized.In this review,we summarize recent progress on characterizing lipid metabolism-related genes and their roles in male fertility and other aspects of reproductive development in plants.On the basis of cloned GMS genes controlling biosynthesis and transport of anther cutin,wax,sporopollenin,and tryphine\r\Arabidopsis,rice,and maize as well as other plant species,updated lipid metabolic networks underlying anther cuticle development and pollen wall formation were proposed.Through bioinformatics analysis of anther RNA-sequencing datasets from three maize inbred lines(Oh43,W23,and B73),a total of 125 novel lipid metabolism-related genes putatively involved in male fertility in maize were deduced.More,we discuss the pathways regulating lipid metabolism-related GMS genes at the transcriptional and post-transcriptional levels.Finally,we highlight recent findings on lipid metabolism-related genes and their roles in other aspects of plant reproductive development.A comprehensive understanding of lipid metabolism,genes involved,and their roles in plant reproductive development will facilitate the application of lipid metabolism-related genes in gene editing,haploid and callus induction,molecular breeding and hybrid seed production in crops.展开更多
Genic male sterility(GMS)is critical for heterosis utilization and hybrid seed production.Although GMS mutants and genes have been studied extensively in plants,it has remained unclear whether chloroplast-associated p...Genic male sterility(GMS)is critical for heterosis utilization and hybrid seed production.Although GMS mutants and genes have been studied extensively in plants,it has remained unclear whether chloroplast-associated photosynthetic and metabolic activities are involved in the regulation of anther development.In this study,we characterized the function of ZmMs33/ZmGPAT6,which encodes a member of the glycerol-3-phosphate acyltransferase(GPAT)family that catalyzes the first step of the glycerolipid synthetic pathway.We found that normal structure and function of endothecium(En)chloroplasts maintained by ZmMs33-mediated lipid biosynthesis in tapetal cells are crucial for maize anther development.ZmMs33 is expressed mainly in the tapetum at early anther developmental stages and critical for cell proliferation and expansion at late stages.Chloroplasts in En cells of wild-type anthers function as starch storage sites before stage 10 but as photosynthetic factories since stage 10 to enable starch metabolism and carbohydrate supply.Loss of ZmMs33 function inhibits the biosynthesis of glycolipids and phospholipids,which are major components of En chloroplast membranes,and disrupts the development and function of En chloroplasts,resulting in the formation of abnormal En chloroplasts containing numerous starch granules.Further analyses reveal that starch synthesis during the day and starch degradation at night are greatly suppressed in the mutant anthers,leading to carbon starvation and low energy status,as evidenced by low trehalose-6-phosphate content and a reduced ATP/AMP ratio.The energy sensor and inducer of autophagy,SnRK1,was activated to induce early and excessive autophagy,premature PCD,and metabolic reprogramming in tapetal cells,finally arresting the elongation and development of mutant anthers.Taken together,our results not only show that ZmMs33 is required for normal structure and function of En chloroplasts but also reveal that starch metabolism and photosynthetic activities of En chloroplasts at different developmental stages are essential for normal anther development.These findings provide novel insights for understanding how lipid biosynthesis in the tapetum,the structure and function of En chloroplasts,and energy and substance metabolism are coordinated to maintain maize anther development.展开更多
APPLICABLE CROP DGMS TECHNOLOGY IN THE POST-HETEROSIS UTILIZATION ERA,The global population is predicted to grow by 25%and reach 10 billion by the mid-21st century(Hickey et al.,2019).To meet the food demands of the g...APPLICABLE CROP DGMS TECHNOLOGY IN THE POST-HETEROSIS UTILIZATION ERA,The global population is predicted to grow by 25%and reach 10 billion by the mid-21st century(Hickey et al.,2019).To meet the food demands of the growing population with limited agricultural land and fresh water resources,greater and more consistent crop production under fluctuating climate conditions,including various environmental stresses,must be achieved by reducing resource inputs and minimizing environmental impacts(Bailey-Serres et al.t 2019).Thanks to the extensive use of semi-dwarf Green Revolution varieties and single-cross hybrids of major crops(e.g.,rice and maize),grain yield has increased steeply over the past 60 years(Figure 1A and 1B).For example。展开更多
基金supported by the National Key Research and Development Program of China(2018YFD0100806,2017YFD0101201 and 2017YFD0102001)the National Natural Science Foundation of China(31871702,31971958 and 31771875)+2 种基金the Fundamental Research Funds for the Central Universities of China(06500136)the Beijing Science&Technology Plan Program(Z191100004019005)。
文摘Sugar metabolism plays an essential role in plant male reproduction. Defects in sugar metabolism during anther and pollen development often result in genic male sterility(GMS). In this review, we summarize the recent progresses of the sugar metabolism-related GMS genes and their roles during plant anther and pollen development, including callose wall and primexine formation, intine development, pollen maturation and starch accumulation, anther dehiscence, and pollen germination and tube growth. We predict 112 putative sugar metabolic GMS genes in maize based on bioinformatics and RNA-seq analyses, and most of them have peak expression patterns during middle or late anther developmental stages.Finally, we outline the potential applications of sugar metabolic GMS genes in crop hybrid breeding and seed production. This review will deepen our understanding on sugar metabolic pathways in controlling pollen development and male fertility in plants.
文摘1.Introduction Global food security faces a severe challenge,as world population is predicted to grow by 25%and reach 10 billion by the mid-21 st century[1].With limited agricultural land and fresh water,greater and more sustainable crop production needs to be achieved by use of modern agricultural technologies[2,3].Among these are developing and exploiting more efficient heterosis utilization strategy with male sterile lines for hybrid breeding and seed production.
基金supported by the National Key Research and Development Program of China(2022YFF1003500 to X.Wan,2022YFF1002400 and 2021YFF1000302 to S.W.,and 2022YFF1100501 to X.Wei)the National Natural Science Foundation of China(31771875 to X.Wan,31900610 to Q.H.31971958 to X.A.,and 31871702 to S.W.)+1 种基金the Fundamental Research Funds for the Central Universities of China(06500136 to X.Wan)the Beijing Nova Program(Z201100006820114 to Q.H.).
文摘Because of its significance for plant male fertility and,hence,direct impact on crop yield,pollen exine development has inspired decades of scientific inquiry.However,the molecularmechanismunderlying exine formation and thickness remains elusive.In this study,we identified that a previously unrecognized repressor,ZmMS1/ZmLBD30,controls proper pollen exine development in maize.Using an ms1 mutant with aberrantly thickened exine,we cloned a male-sterility gene,ZmMs1,which encodes a tapetum-specific lateral organ boundary domain transcription factor,ZmLBD30.Weshowed thatZmMs1/ZmLBD30 is initially turned on by a transcriptional activation cascade of ZmbHLH51-ZmMYB84-ZmMS7,and then it serves as a repressor to shut down this cascade via feedback repression to ensure timely tapetal degeneration and proper level of exine.This activation-feedback repression loop regulating male fertility is conserved in maize and sorghum,and similar regulatory mechanism may also exist in other flowering plants such as rice and Arabidopsis.Collectively,these findings reveal a novel regulatory mechanism of pollen exine development by which a long-sought master repressor of upstream activators prevents excessive exine formation.
基金the National Key Research and Development Program of China (2018YFD0100806,2017YFD0102001,2017YFD0101201)the National Transgenic Major Program of China (2018ZX0801006B,2018ZX0800922B)+6 种基金the National Natural Science Foundation of China (31771875,31871702)the Fundamental Research Funds for the Central Universities of China (06500060FRF-BR-17- 009A,-010Aand -011 A)the "Ten Thousand Plann-National High Level Talents Special Support Plan (for X.W.)the National Key Technology R&D Program of China (2014BAD01B02)and the Beijing Science & Technology Plan Program (Z161100000916013).
文摘Genic male sterility (GMS) is very useful for hybrid vigor utilization and hybrid seed production. Although a large number of GMS genes have been identified in plants, little is known about the roles of GDSL lipase members in anther and pollen development. Here, we report a maize GMS gene, ZmMs30, which encodes a novel type of GDSL lipase with diverged catalytic residues. Enzyme kinetics and activity assays show that ZmMs30 has lipase activity and prefers to substrates with a short carbon chain. ZmMs30 is specifically expressed in maize anthers during stages 7-9. Loss of ZmMs30 function resulted in defective anther cuticle, irregular foot layer of pollen exine, and complete male sterility. Cytological and lipidomics analyses demonstrate that ZmMs30 is crucial for the aliphatic metabolic pathway required for pollen exine formation and anther cuticle development. Furthermore, we found that male sterility caused by loss of ZmMs30 function was stable in various inbred lines with different genetic background, and that it didn't show any negative effect on maize heterosis and production, suggesting that ZmMs30 is valuable for crossbreeding and hybrid seed production. We then developed a new multi-control sterility system using ZmMs30 and its mutant line, and demonstrated it is feasible for generating desirable GMS lines and valu. able for hybrid maize seed production. Taken together, our study sheds new light on the mechanisms of anther and pollen development, and provides a valuable male-sterility system for hybrid breeding maize.
基金the National Transgenic Major Program of China (2018ZX0801006B,2018ZX0800922B)the National Key Research and Development Program of China (2018YFD0100806,2017YFD0102001,2017YFD0101201)+6 种基金the National Natural Science Foundation of China (31771875,31871702)the Fundamental Research Funds for the Central Universities of China (06500060FRF-BR-17-009AFRF-BR-17-010AFRF-BR-17-011A)the "Ten Thousand Plan”- National High Level Talents Special Support Plan (For X.W.)and the Beijing Science & Technology Plan Program (Z161100000916013).
文摘As one of the most important crops, maize not only has been a source of the food, feed, and industrial feedstock for biofuel and bioproducts, but also became a model plant system for addressing fundamental questions in genetics. Male sterility is a very useful trait for hybrid vigor utilization and hybrid seed production. The identification and characterization of genic male-sterility (GMS) genes in maize and other plants have deepened our understanding of the molecular mechanisms controlling anther and pollen development, and enabled the development and efficient use of many biotechnology-based male-sterility (BMS) systems for crop hybrid breeding. In this review, we summarize main advances on the identification and characterization of GMS genes in maize, and con struct a putative regulatory network controlling maize anther and pollen development by comparative genomic analysis of GMS genes in maize, Arabidopsis, and rice. Furthermore, we discuss and appraise the features of more than a dozen BMS systems for propagating male-sterile lines and producing hybrid seeds in maize and other plants. Finally, we provide our perspectives on the studies of GMS genes and the development of novel BMS systems in maize and other plants. The continuous exploration of GMS genes and BMS systems will enhance our understanding of molecular regulatory networks controlling male fertility and greatly facilitate hybrid vigor utilization in breeding and field production of maize and other crops.
基金This research was supported by the National Transgenic Major Program of China(2018ZX08010-06B,2018ZX08009-22B)the National Key Research and Development Program of China(2017YFD0102001,2018YFD0100806,2017YFD0101201)+2 种基金the National Natural Science Foundation of China(31971958,31771875,31871702)the Fundamental Research Funds for the Central Universities of China(06500136)the"Ten Thousand Plan"-National High Level Talents Special Support Plan(For X.W.),and the Beijing Science&Technology Plan Program(Z191100004019005).
文摘Fatty acids and their derivatives are essential building blocks for anther cuticle and pollen wall formation.Disruption of lipid metabolism during anther and pollen development often leads to genic male sterility(GMS).To date,many lipid metabolism-related GMS genes that are involved in the formation of anther cuticle,pollen wall,and subcellular organelle membranes in anther wall layers have been identified and characterized.In this review,we summarize recent progress on characterizing lipid metabolism-related genes and their roles in male fertility and other aspects of reproductive development in plants.On the basis of cloned GMS genes controlling biosynthesis and transport of anther cutin,wax,sporopollenin,and tryphine\r\Arabidopsis,rice,and maize as well as other plant species,updated lipid metabolic networks underlying anther cuticle development and pollen wall formation were proposed.Through bioinformatics analysis of anther RNA-sequencing datasets from three maize inbred lines(Oh43,W23,and B73),a total of 125 novel lipid metabolism-related genes putatively involved in male fertility in maize were deduced.More,we discuss the pathways regulating lipid metabolism-related GMS genes at the transcriptional and post-transcriptional levels.Finally,we highlight recent findings on lipid metabolism-related genes and their roles in other aspects of plant reproductive development.A comprehensive understanding of lipid metabolism,genes involved,and their roles in plant reproductive development will facilitate the application of lipid metabolism-related genes in gene editing,haploid and callus induction,molecular breeding and hybrid seed production in crops.
基金the National Key Research and Development Program of China(2017YFD0102001,2018YFD0100806,2017YFD0101201)the National Transgenic Major Program of China(2018ZX0801006B,2018ZX0800922B)+3 种基金the National Natural Science Foundation of China(31971958,31771875,31871702)the Fundamental Research Funds for the Central Universities of China(06500136)the"Ten Thousand Plan"-National High Level Talents Special Support Plan(to X.W.)the Beijing Science&Technology Plan Program(Z191100004019005).
文摘Genic male sterility(GMS)is critical for heterosis utilization and hybrid seed production.Although GMS mutants and genes have been studied extensively in plants,it has remained unclear whether chloroplast-associated photosynthetic and metabolic activities are involved in the regulation of anther development.In this study,we characterized the function of ZmMs33/ZmGPAT6,which encodes a member of the glycerol-3-phosphate acyltransferase(GPAT)family that catalyzes the first step of the glycerolipid synthetic pathway.We found that normal structure and function of endothecium(En)chloroplasts maintained by ZmMs33-mediated lipid biosynthesis in tapetal cells are crucial for maize anther development.ZmMs33 is expressed mainly in the tapetum at early anther developmental stages and critical for cell proliferation and expansion at late stages.Chloroplasts in En cells of wild-type anthers function as starch storage sites before stage 10 but as photosynthetic factories since stage 10 to enable starch metabolism and carbohydrate supply.Loss of ZmMs33 function inhibits the biosynthesis of glycolipids and phospholipids,which are major components of En chloroplast membranes,and disrupts the development and function of En chloroplasts,resulting in the formation of abnormal En chloroplasts containing numerous starch granules.Further analyses reveal that starch synthesis during the day and starch degradation at night are greatly suppressed in the mutant anthers,leading to carbon starvation and low energy status,as evidenced by low trehalose-6-phosphate content and a reduced ATP/AMP ratio.The energy sensor and inducer of autophagy,SnRK1,was activated to induce early and excessive autophagy,premature PCD,and metabolic reprogramming in tapetal cells,finally arresting the elongation and development of mutant anthers.Taken together,our results not only show that ZmMs33 is required for normal structure and function of En chloroplasts but also reveal that starch metabolism and photosynthetic activities of En chloroplasts at different developmental stages are essential for normal anther development.These findings provide novel insights for understanding how lipid biosynthesis in the tapetum,the structure and function of En chloroplasts,and energy and substance metabolism are coordinated to maintain maize anther development.
基金This research was supported by the National Key Research and Development Program of China(2018YFD0100806,2018YFD1000702,2017YFD0102001,2017YFD0101201)the National Natural Science Foundation of China(31771875,31871702,31971958)the Fundamental Research Funds for the Central Universities of China(06500136).
文摘APPLICABLE CROP DGMS TECHNOLOGY IN THE POST-HETEROSIS UTILIZATION ERA,The global population is predicted to grow by 25%and reach 10 billion by the mid-21st century(Hickey et al.,2019).To meet the food demands of the growing population with limited agricultural land and fresh water resources,greater and more consistent crop production under fluctuating climate conditions,including various environmental stresses,must be achieved by reducing resource inputs and minimizing environmental impacts(Bailey-Serres et al.t 2019).Thanks to the extensive use of semi-dwarf Green Revolution varieties and single-cross hybrids of major crops(e.g.,rice and maize),grain yield has increased steeply over the past 60 years(Figure 1A and 1B).For example。