Altered sucrose metabolism and gene regulation in wheat (Triticum aestivum) K-type cytoplasmic male sterility
Qingsong Ba![https://orcid.org/0000-0003-3637-4672](/media/client/orcid_16x16.png)
A School of Life Science, Huaibei Normal University, Key Laboratory of Plant Resources and Biology of Anhui Province, Huaibei, 235000 Anhui, P.R. China.
B Key Laboratory of Crop Heterosis of Shaanxi Province, Northwest A&F University, Yangling, 712100 Shaanxi, P.R. China.
C Zhoukou Normal University, Zhoukou, 466001 Henan, P.R. China.
D Corresponding author. Email: baqs1234@163.com
Crop and Pasture Science 70(3) 204-210 https://doi.org/10.1071/CP18517
Submitted: 15 November 2018 Accepted: 22 January 2019 Published: 12 March 2019
Abstract
K-Type cytoplasmic male sterility (K-CMS) plays an important role in breeding hybrid wheat. This study was designed to investigate the association of sucrose metabolism with K-CMS in wheat (Triticum aestivum L.) anthers at the binucleate stage. Levels of sucrose in the anthers of the K-CMS line remained higher than in the fertile line, but glucose and fructose contents in the anthers of the K-CMS line were dramatically lower than in the fertile line. Compared with the fertile line, the activities of cell-wall-bound invertase (CWIN), neutral invertase and vacuolar invertase (VIN) were significantly reduced. Quantitative real-time polymerase chain reaction analyses showed that the expression levels of one CWIN gene (IVR1), one VIN gene (IVR5) and a sucrose transporter gene (TaSUT1) were significantly downregulated in K-CMS anthers. Furthermore, western blot confirmed that the protein expression level of IVR1 was higher in sterile anthers than in male fertile anthers. Thus, it appears that the accumulation of sucrose in K-CMS anthers might involve a decrease in activity and a reduction in content of invertase. In conclusion, the results suggest that an inability to metabolise incoming sucrose to hexoses may be involved in the K-CMS pollen-developmental lesion.
Additional keywords: invertase, male sterility, qPCR, sucrose metabolism, wheat.
References
Ba Q, Zhang G, Che H, Liu H, Ng TB, Zhang L, Wang J, Sheng Y, Niu N, Ma S (2014a) Aliphatic metabolism during anther development interfered by chemical hybridizing agent in wheat. Crop Science 54, 1458–1467.| Aliphatic metabolism during anther development interfered by chemical hybridizing agent in wheat.Crossref | GoogleScholarGoogle Scholar |
Ba Q, Zhang G, Niu N, Ma S, Wang J (2014b) Cytoplasmic effects on DNA methylation between male sterile lines and the maintainer in wheat (Triticum aestivum L.). Gene 549, 192–197.
| Cytoplasmic effects on DNA methylation between male sterile lines and the maintainer in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 24875418PubMed |
Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J, Hedrich R (2005) Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. The Journal of Biological Chemistry 280, 21437–21443.
| Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force.Crossref | GoogleScholarGoogle Scholar | 15805107PubMed |
Castro AJ, Clément C (2007) Sucrose and starch catabolism in the anther of Lilium during its development: a comparative study among the anther wall, locular fluid and microspore/pollen fractions. Planta 225, 1573–1582.
| Sucrose and starch catabolism in the anther of Lilium during its development: a comparative study among the anther wall, locular fluid and microspore/pollen fractions.Crossref | GoogleScholarGoogle Scholar | 17123100PubMed |
Cheng J, Wang Z, Yao F, Gao L, Ma S, Sui X, Zhang Z (2015) Down-regulating CsHT1, a cucumber pollen-specific hexose transporter, inhibits pollen germination, tube growth, and seed development. Plant Physiology 168, 635–647.
| Down-regulating CsHT1, a cucumber pollen-specific hexose transporter, inhibits pollen germination, tube growth, and seed development.Crossref | GoogleScholarGoogle Scholar | 25888616PubMed |
Chung P, Hsiao HH, Chen HJ, Chang CW, Wang SJ (2014) Influence of temperature on the expression of the rice sucrose transporter 4 gene, OsSUT4, in germinating embryos and maturing pollen. Acta Physiologiae Plantarum 36, 217–229.
| Influence of temperature on the expression of the rice sucrose transporter 4 gene, OsSUT4, in germinating embryos and maturing pollen.Crossref | GoogleScholarGoogle Scholar |
Cui P, Liu H, Lin Q, Ding F, Zhuo G, Hu S, Liu D, Yang W, Zhan K, Zhang A (2009) A complete mitochondrial genome of wheat (Triticum aestivum cv. Chinese Yumai), and fast evolving mitochondrial genes in higher plants. Journal of Genetics 88, 299–307.
| A complete mitochondrial genome of wheat (Triticum aestivum cv. Chinese Yumai), and fast evolving mitochondrial genes in higher plants.Crossref | GoogleScholarGoogle Scholar | 20086295PubMed |
Datta R, Chamusco KC, Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiology 130, 1645–1656.
| Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize.Crossref | GoogleScholarGoogle Scholar | 12481048PubMed |
Eom JS, Cong DN, Lee DW, Lee SK, Jeon JS (2016) Genetic complementation analysis of rice sucrose transporter genes in Arabidopsis SUC2 mutant atsuc2. Journal of Plant Biology 59, 231–237.
| Genetic complementation analysis of rice sucrose transporter genes in Arabidopsis SUC2 mutant atsuc2.Crossref | GoogleScholarGoogle Scholar |
Garrido D, Busscher J, van Tunen AJ (2006) Promoter activity of a putative pollen monosaccharide transporter in Petunia hybrida and characterisation of a transposon insertion mutant. Protoplasma 228, 3–11.
| Promoter activity of a putative pollen monosaccharide transporter in Petunia hybrida and characterisation of a transposon insertion mutant.Crossref | GoogleScholarGoogle Scholar | 16937049PubMed |
Goetz M, Godt DE, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proceedings of the National Academy of Sciences of the United States of America 98, 6522–6527.
| Induction of male sterility in plants by metabolic engineering of the carbohydrate supply.Crossref | GoogleScholarGoogle Scholar | 11371651PubMed |
Gong Y, Liu Y, Gao J (2004) Growth analysis on the process of grain filling in hybrid wheat 901 and its parents. Scientia Agricultura Sinica 37, 1288–1292.
Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B, Kühn C (2006) Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. The Plant Journal 45, 180–192.
| Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways.Crossref | GoogleScholarGoogle Scholar | 16367963PubMed |
Hirose T, Zhang Z, Miyao A, Hirochika H, Ohsugi R, Terao T (2010) Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected. Journal of Experimental Botany 61, 3639–3646.
| Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected.Crossref | GoogleScholarGoogle Scholar | 20603282PubMed |
Hirsche J, Engelke T, Völler D, Götz M, Roitsch T (2009) Interspecies compatibility of the anther specific cell wall invertase promoters from Arabidopsis and tobacco for generating male sterile plants. Theoretical and Applied Genetics 118, 235–245.
| Interspecies compatibility of the anther specific cell wall invertase promoters from Arabidopsis and tobacco for generating male sterile plants.Crossref | GoogleScholarGoogle Scholar | 18825361PubMed |
Huang CZ, Liu XL, Cao RF, Zhao HX (2017) Prokaryotic expression, purification and preparation of polyclonal antibody for wheat (Triticum aestivum L.) CWI-B1. Journal of Agricultural Biotechnology 25, 1102–1110.
Ji X, Shiran B, Wan J, Lewis DC, Jenkins CL, Condon AG, Richards RA, Dolferus R (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant, Cell & Environment 33, 926–942.
| Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat.Crossref | GoogleScholarGoogle Scholar |
Kihara H (1951) Substitution of nucleus and its effects on genome manifestations. Cytologia 16, 177–193.
| Substitution of nucleus and its effects on genome manifestations.Crossref | GoogleScholarGoogle Scholar |
Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiology 148, 1523–1536.
| Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria.Crossref | GoogleScholarGoogle Scholar | 18784281PubMed |
Koonjul PK, Minhas JS, Nunes C, Sheoran IS, Saini HS (2005) Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat. Journal of Experimental Botany 56, 179–183.
Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant, Cell & Environment 26, 37–56.
| Phloem loading and unloading of sugars and amino acids.Crossref | GoogleScholarGoogle Scholar |
Liu H, Peng C, Zhan K, Qiang L, Zhuo G, Guo X, Feng D, Yang W, Liu D, Hu S (2011) Comparative analysis of mitochondrial genomes between a wheat K-type cytoplasmic male sterility (CMS) line and its maintainer line. BMC Genomics 12, 163–168.
| Comparative analysis of mitochondrial genomes between a wheat K-type cytoplasmic male sterility (CMS) line and its maintainer line.Crossref | GoogleScholarGoogle Scholar | 21443807PubMed |
Milne RJ, Perroux JM, Rae AL, Reinders A, Ward JM, Offler CE, Patrick JW, Grof CP (2017) Sucrose transporter localization and function in phloem unloading in developing stems. Plant Physiology 173, 1330–1341.
| Sucrose transporter localization and function in phloem unloading in developing stems.Crossref | GoogleScholarGoogle Scholar | 27986867PubMed |
Mukai Y, Tsunewaki K (1979) Basic studies on hybrid wheat breeding. Theoretical and Applied Genetics 54, 153–160.
| Basic studies on hybrid wheat breeding.Crossref | GoogleScholarGoogle Scholar | 24310337PubMed |
Nguyen GN, Hailstones DL, Wilkes M, Sutton BG (2010) Role of carbohydrate metabolism in drought-induced male sterility in rice anthers. Journal of Agronomy & Crop Science 196, 346–357.
| Role of carbohydrate metabolism in drought-induced male sterility in rice anthers.Crossref | GoogleScholarGoogle Scholar |
Ohdan T, Francisco PJT, Hirose T, Terao T, Satoh H, Nakamura Y (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. Journal of Experimental Botany 56, 3229–3244.
| Expression profiling of genes involved in starch synthesis in sink and source organs of rice.Crossref | GoogleScholarGoogle Scholar | 16275672PubMed |
Oliver SN, Van Dongen JT, Alfred SC, Mamun EA, Zhao X, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant, Cell & Environment 28, 1534–1551.
| Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility.Crossref | GoogleScholarGoogle Scholar |
Oliver SN, Dennis ES, Dolferus R (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant & Cell Physiology 48, 1319–1330.
| ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice.Crossref | GoogleScholarGoogle Scholar |
Poschet G, Hannich B, Büttner M (2010) Identification and characterization of AtSTP14, a novel galactose transporter from Arabidopsis. Plant & Cell Physiology 51, 1571–1580.
| Identification and characterization of AtSTP14, a novel galactose transporter from Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends in Plant Science 9, 606–613.
| Function and regulation of plant invertases: sweet sensations.Crossref | GoogleScholarGoogle Scholar | 15564128PubMed |
Saini HS, Westgate ME (2000) Reproductive development in grain crops during drought. Advances in Agronomy 68, 59–96.
Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Letters 581, 2309–2317.
| Molecular physiology of higher plant sucrose transporters.Crossref | GoogleScholarGoogle Scholar | 17434165PubMed |
Schneidereit A, Scholz-Starke J, Büttner M (2003) Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis. Plant Physiology 133, 182–190.
| Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12970485PubMed |
Singh SK, Chatrath R, Mishra B (2010) Perspective of hybrid wheat research: A review. Indian Journal of Agricultural Sciences 12, 1013–1027.
| Perspective of hybrid wheat research: A review.Crossref | GoogleScholarGoogle Scholar |
Sivitz AB, Reinders A, Ward JM (2008) Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose-induced anthocyanin accumulation. Plant Physiology 147, 92–100.
| Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose-induced anthocyanin accumulation.Crossref | GoogleScholarGoogle Scholar | 18359840PubMed |
Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiology 139, 701–712.
| Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos.Crossref | GoogleScholarGoogle Scholar | 16169962PubMed |
Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiology 121, 1–8.
| Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning.Crossref | GoogleScholarGoogle Scholar | 10482654PubMed |
Tada Y (2007) Effects of Rf-1, Rf-3 and Rf-6(t) genes on fertility restoration in rice (Oryza sativa L.) with WA- and BT-type cytoplasmic male sterility. Breeding Science 57, 223–229.
| Effects of Rf-1, Rf-3 and Rf-6(t) genes on fertility restoration in rice (Oryza sativa L.) with WA- and BT-type cytoplasmic male sterility.Crossref | GoogleScholarGoogle Scholar |
Wu Z, Cheng J, Qin C, Hu Z, Yin C, Hu K (2013) Differential proteomic analysis of anthers between cytoplasmic male sterile and maintainer lines in Capsicum annuum L. International Journal of Molecular Sciences 14, 22982–22996.
| Differential proteomic analysis of anthers between cytoplasmic male sterile and maintainer lines in Capsicum annuum L.Crossref | GoogleScholarGoogle Scholar | 24264042PubMed |
Yang W, Lou X, Li J, Pu M, Mirbahar AA, Liu D, Sun J, Zhan K, He L, Zhang A (2017) Cloning and functional analysis of MADS-box genes, TaAG-A and TaAG-B, from a wheat K-type cytoplasmic male sterile line. Frontiers of Plant Science 8, 1081–1089.
| Cloning and functional analysis of MADS-box genes, TaAG-A and TaAG-B, from a wheat K-type cytoplasmic male sterile line.Crossref | GoogleScholarGoogle Scholar |
Yao Y, Zhang G, Liu H, Wang J (2003) Cytomorphology and cytochemical localization of K-type and T-type cytoplasmic male sterile pollens in wheat. Journal of Integrative Agriculture 2, 591–596.
Ylstra B, Garrido D, Busscher J, van Tunen AJ (1998) Hexose transport in growing petunia pollen tubes and characterization of a pollen-specific, putative monosaccharide transporter. Plant Physiology 118, 297–304.
| Hexose transport in growing petunia pollen tubes and characterization of a pollen-specific, putative monosaccharide transporter.Crossref | GoogleScholarGoogle Scholar | 9733549PubMed |
Yuan JS, Reed A, Chen F, Stewart CN (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85–90.
| Statistical analysis of real-time PCR data.Crossref | GoogleScholarGoogle Scholar | 16504059PubMed |
Zanor MI, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kühn C, Bleiss W, Giavalisco P, Willmitzer L, Sulpice R, Zhou Y-H, Fernie AR (2009) RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiology 150, 1204–1218.
| RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility.Crossref | GoogleScholarGoogle Scholar | 19439574PubMed |
Zhang F, Li G, Ding Q, Wang Z, Ma X, Zhang H, Zhang Z, Jin F, Ma L (2016) Proteome analysis of pollen in the K-type male sterility line 732A and its maintainer 732B in wheat (Triticum aestivum L.) by two-dimensional gel electrophoresis. Acta Physiologiae Plantarum 38, 84–90.
| Proteome analysis of pollen in the K-type male sterility line 732A and its maintainer 732B in wheat (Triticum aestivum L.) by two-dimensional gel electrophoresis.Crossref | GoogleScholarGoogle Scholar |
Zhu W, Ma S, Zhang G, Liu H, Ba Q, Li Z, Song Y, Zhang P, Niu N, Wang J (2015) Carbohydrate metabolism and gene regulation during anther development disturbed by chemical hybridizing agent in wheat. Crop Science 55, 868–876.
| Carbohydrate metabolism and gene regulation during anther development disturbed by chemical hybridizing agent in wheat.Crossref | GoogleScholarGoogle Scholar |