Transcriptomic Microarray Analysis Revealed Acetyl-CoA Metabolic Pathway Defect in Male Sterile Line BNS in Wheat (Triticum aestivum)
FU Qing-Yun1, YANG Jing1, SUN Hai-Li1, SU Qing1,2, WEI Xiao1, RU Zhen-Gang1*, LI You-Yong1*
1 School of Life Science and Technology, Henan Institute of Science and Technology/Collaborative Innovation Center of Modern Biological Breeding, Xinxiang 453003, China; 2 College of Life Science, Henan Normal University, Xinxiang 453003, China
Abstract BNS (Bai-nong sterility) is a nuclear thermo-sensitive male sterile line of common wheat (Triticum aestivum), which plays an important role for the study of hybrid wheat. In order to explore the physiological mechanism of BNS sterility, Affymetrix wheat microarray was used to detect the transcriptomes of BNS male sterility and male fertile in anthers and spike-stalks in the developmental stage of tetrad and mononuclear, and analyzed metabolic networks generated by differential probe genes. The results found that an acetyl-CoA metabolic sub-network could be formed in the profiles of up-regulated genes in fertile anthers, but the sub- network was incompletely in partly sterile anthers, and it was not formed in sterile anthers. The acetyl-CoA sub-metabolic network consisted of 6 nodes, which were acetyl-CoA synthesis and metabolism, acyl-CoA synthesis and metabolism, and thioester synthesis and metabolism, respectively. The nodes of sub-network of acetyl-CoA first linked to that of hormone metabolism, waxy metabolism, amino acid metabolism and linked to ATP synthesis, mitochondrial electron transfer, and so on, then connected with stigma and anther development. Acetyl-CoA was a pivotal substance in cell energy metabolism, so the deficiency of this metabolic pathway directly affected the production of energy carriers such as ATP, thus affecting microspore development. ATP content in anther and flag leaf tissue of BNS sterile and fertile plants were detected, respectively. The results showed the content of ATP in the sterile anther decreased by about 10% compared with fertile anther (P<0.01), and the content of ATP in the sterile flag leaf decreased by 50% compared with fertile flag leaf (P<0.01). The results indicated that there was a shortage of ATP supply in the critical period of microspore development. Thus it was believed that the metabolic defect of acetyl-CoA was an important physiological mechanism for BNS male sterility. The mechanism provides an important clue for revealing the occurrence of BNS infertility.
FU Qing-Yun,YANG Jing,SUN Hai-Li, et al. Transcriptomic Microarray Analysis Revealed Acetyl-CoA Metabolic Pathway Defect in Male Sterile Line BNS in Wheat (Triticum aestivum)[J]. 农业生物技术学报, 2023, 31(4): 682-694.
[1] 曹银萍, 杨靖, 卫笑, 等. 2019. 小麦 BNS 雄性不育显性遗传方式的观察与分析[J]. 中国农业科技导报, 21(7): 19-30. (Cao Y P, Yang J, Wei X, et al. 2019. Observation and analysis of dominant genetic pattern of BNS male sterility in wheat (Triticum aestivum L)[J]. Journal of Ag-ricultural Science and Technology, 21(7): 19-30. ) [2] 高金玉, 韩冰, 杨晓虹, 等. 2017. 禾本科植物雄性不育遗传机制与利用[J]. 北方农业学报, 45(1): 25-32. (Gao J Y, Han B, Yang X H, et al. 2017. Genetic mechanism and utilization of the Gramineae male sterile[J]. Journal of Northern Agriculture), 45(1): 25-32. ) [3] 李罗江, 茹振刚, 高庆荣, 等. 2009a. BNS 小麦的雄性不育性及其温光特性[J]. 中国农业科学, 42(9): 3019-3027. (Li L J, Ru Z G, Gao Q R, et al. 2009. Male sterility and thermo-photosensitivity characteristics of BNS in wheat[J]. Scientia Agricultura Sinica, 42(9): 3019-3027. ) [4] 李罗江, 茹振钢, 高庆荣, 等. 2009b. 小麦雄性不育系 BNS及其杂种 F1 的育性分析[J]. 麦类作物学报, 29(4): 583-587. (Li L J, Ru Z G, Gao Q R, et al. 2009. Analysis the fertility of male-sterile line BNS and its F1 hybrids in wheat[J]. Journal of Triticeae Crops, 29(4): 583-587. ) [5] 李友勇, 茹振刚, 苏晴, 等. 2011. 小麦 BNS 雄性不育系及其转换系花药差异蛋白鉴定与分析[J]. 作物学报, 37(9): 1540-1550. (Li Y Y, Ru Z G, Su Q, et al. 2011. Differen-tially expressed proteins of BNS male sterile line and its conversion line of wheat[J]. Acta Agronomica Sinica, 37(9): 1540-1550. ) [6] 苗锦山, 杨文才, 刘彩霞,等. 2010. 葱胞质雄性不育花蕾生化物质含量和能量代谢酶活性的动态变化特征[J]. 西北植物学报, 30(6): 1142-1148. (Miao J S, Yang W C, Liu C X, et al. 2010. Dynamic changes of physiological and biochemical substances and energy metabolism en-zyme activities in bud of welsh onion CMS line[J]. Acta Botanica Boreali-Occidentalia Sinica, 2010, 30(6): 1142-1148. ) [7] 秦志英, 孙海燕, 付庆云, 等. 2018. 冬春温度变化对小麦温敏雄性不育系 BNS 的育性转换影响[J]. 西北农业学报, 27(1): 31-37. (Qin Z Y, Sun H Y, Fu Q Y, et al. 2018. Study on significant effects of temperature changes in winter and spring on fertility conversion in wheat ther-mo-sensitive male sterile line BNS[J]. Acta Agriculturae Boreali-occidentalis Sinica, 27(1): 31-37. ) [8] 苏晴, 秦志英, 程威, 等. 2011. 小麦 BNS 雄性不育系小孢子发育形态结构的细胞学观察[J]. 河南科技学院学报, 39(6): 5-9. (Su Q, Qin Z Y, Cheng, W, et al. 2011. Mor-phological and structural observations on anther and mi-crospore developments of male sterile line BNS in wheat[J]. Journal of Henan Institute of Science and Technolo-gy), 39(6): 5-9. ) [9] 苏晴, 茹振钢, 秦志英, 等. 2013. 小热激蛋白基因(hsp23. 5)在小麦 BNS 雄性不育系和转换系中的差异表达[J]. 农业生物技术学报, 21(1): 29-37. (Su Q, Ru Z G, Qin Z Y, et al. 2013. Differential expression of small heat shock protein gene (hsp23. 5) between wheat (Triticum aestivum L. ) BNS male sterile line and its conversion line[J]. Journal of Agricultural Biotechnology, 21(1): 29-37. ) [10] 孙海燕, 贾菲芸, 杨靖, 等. 2020. 小麦 BNS 雄性不育系晚霜冻抗性和低温不育特性观察[J]. 麦类作物学报, 40(9): [11] 1041-1047. (Sun H Y, Jia F Y, Yang J, et al. 2020. Obser-vation on late frost resistance and low temperature steril-ity of the BNS male sterile line in wheat[J]. Journal of Triticeae Crops, 40(9): 1041-1047. ) [12] 孙慧慧, 杨靖, 卫笑, 等. 2016. 小麦 BNS 雄性不育中国春恢复基因的连锁群检测和 QTL 初步定位[J]. 麦类作物学报, 36(7): 856-865. (Sun H H, Yang J, Wei X, et al. 2016. Detection of linkage groups and location of QTLs in Chinese Spring for restoring wheat BNS male sterility[J]. Journal of Triticeae Crops), 36(7): 856-865. ) [13] 王茂婷, 高庆荣, 孙正娟, 等. 2011. BNS 小麦穗分化进程与其雄性不育性的表现[J]. 分子植物育种, 9(3): 294-301. (Wang M T, Gao Q R, Sun Z J, et al. 2011. Spike differentiation process and the male sterility of BNS in wheat[J]. Molecular Plant Breeding, 9(3): 294-301. ) [14] 王秀珍, 滕晓月, 阎隆飞, 等. 1986. 玉米及高粱花药中三磷酸腺苷(ATP)含量与细胞质雄性不育的关系[J]. 作物学报, 12(3): 177-181. (Wang X Z, Teng X Y, Yan L F, et al. 1986. The relationship between the ATP content in anthers of maize and sorghum and cytoplasmic male-ste-rility[J]. Acta Agronomica Sinica, 12(3): 177-181. ) [15] 王震, 范晓静, 张淼, 等. 2014. ATP 合成相关基因在小麦 BNS 不育系育性转换中的差异表达[J]. 作物学报, 40(8): 1501-1505. (Wang Z, Fan X J, Zhang M, et al. 2014. Differential expression of ATP synthesis related gene in fertility conversion of wheat BNS male sterile line[J]. Acta Agronomica Sinica, 40(8): 1501-1505. ) [16] 张江江, 常丽, 赵立宁, 等. (2019). 雄性不育中花粉壁的研究进展[J]. 生物技术通报, 35(6): 138-146. (Zhang J J, Chang L, Zhao L N, et al. Research advance on pollen wall development in male sterility[J]. Biotechnology Bulletin, 35(6): 138-146. ) [17] 张兰军, 张保才, 周奕华. 2018. 植物细胞壁多糖乙酰化修饰与生物学功能[J]. 植物生理学报, 54(8): 1272-1278. (Zhang L J, Zhang B C, Zhou Y H. Progress on polysac-charide acetylation in plant cell wall[J]. Plant Physiolo-gy Journal, 54(8): 1272-1278. ) [18] 张蕊, 李来庚. 2018. 植物细胞壁信号研究进展[J]. 植物生理学报, 54(8): 1254-1262. (Zhang R, Li L G. 2018. Re-search progress of the plant cell wall signaling[J]. Plant Physiology Journal, 54(8): 1254-1262. ) [19] 张自阳, 胡铁柱, 茹振钢, 等. 2010. 温敏核雄性不育小麦 BNS 的育性转换规律初探[J]. 河南农业科学, (7): 5-9. (Zhang Z Y, Hu T Z, Ru Z G, et al. 2010. A preliminary study on fertility alteration of thermo-sensitive genic male sterile wheat line BNS[J]. Journal of Henan Agri-cultural Science, (7): 5-9. ) [20] 赵大华, 孙慧慧, 于同英, 等. 2014. atp1 基因在小麦 BNS 雄性不育系和自身转换系中的差异表达[J]. 生命科学研究, 18(6): 488-493. (Zhao D H, Sun H H, Yu T Y, et al. 2014. Gene atp1 expresses differentially between BNS male sterile line and its conversion line in wheat[J]. Life Science Research, 18(6): 488-493. ) [21] 周美兰, 茹振钢, 骆叶青, 等. 2010. 两系小麦不育系 BNS 雄性育性的转换[J]. 核农学报, 24(5): 887-894. (Zhou M L, Ru Z G, Luo Y Q, et al. 2010. Male fertility transfor-mation of two-line wheat sterile lines BNS[J]. Journal of Nuclear Agricultural Sciences, 24(5): 887-894. ) [22] 周小利, 杨诗怡, 陈志芸, 等. 2018. 植物细胞质雄性不育和育性恢复基因调控机制研究进展[J]. 农学学报,8(7): 62-67. (Zhou X L, Yang S Y, Chen Z Y, et al. 2018. Reg-ulation mechanism of cytoplasmic male sterility and fer-tility restoration gene in plants research progress[J]. Journal of Agriculture, 8(7): 62-67. ) [23] Bindea G, Mlecnik B, Hackl H, et al. 2009. ClueGO: A cyto-scape plug-in to decipher functionally grouped gene on-tology and pathway annotation networks[J]. Bioinfor-matics, 25(8): 1091-1093. [24] Chen Y N, Lei S L, Zhou Z F, et al. 2009. Analysis of gene ex-pression profile in pollen development of recessive gen-ic male sterile Brassica napus L. line S45A[J]. Plant Cell Reports, 28:1363-1372. [25] Geng X X, Ye J L, Yang X T, et al. 2018. Identification of pro-teins involved in carbohydrate metabolism and energy metabolism pathways and their regulation of cytoplas-mic male sterility in wheat[J]. International Journal of Molecular Sciences, 19: 324. [26] Li J J, Pandeya D, Jo Y D, et al. 2013. Reduced activity of ATP synthase in mitochondria causes cytoplasmic male sterility in chili pepper[J]. Planta, 237: 1097-1109. [27] Li S, Liu Z H, Jia Y L, et al. 2019. Analysis of metabolic path-ways related to fertility restoration and identification of fertility candidate genes associated with Aegilops kotschyi cytoplasm in wheat (Triticum aestivum L. )[J]. BMC Plant Biology, 19: 252. [28] Li Y Y, Li Y, Fu Q Y, et al. 2015. Anthers proteomic character-ization and change in temperature sensitive Bai-nong male sterile wheat (Triticum aestivum L. )[J]. Biologia Plantarum, 59(2): 273-282. [29] Liu J, Pang C Y, Wei H L, et al. 2014. Proteomic analysis of anthers from wild-type and photosensitive genetic male sterile mutant cotton (Gossypium hirsutum L. )[J]. BMC Plant Biology, 14: 390. [30] Shannon P, Markiel A, Ozier O, et al. 2003. Cytoscape: A soft-ware environment for integrated models of biomolecular interaction networks[J]. Genome Research, 13(11): 2498-2504. [31] Shearman J R, Sangsrakru D, Ruang-Areerate P, et al. 2014. Assembly and analysis of a male sterile rubber tree mito-chondrial genome reveals DNA rearrangement events and a novel transcript[J]. BMC Plant Biology, 2014, 14: 45. ) [32] Su Q, Yang J, Fu Q Y, et al. 2019. Profiling of indole metabol-ic pathway in thermo-sensitive Bainong male sterile line in wheat (Triticum aestivum L. )[J]. Physiology and Mo-lecular Biology of Plants, 25(1): 263-275. [33] Wan C X, Li S Q, Wen Let al. 2007. Damage of oxidative stress on mitochondria during microspores development in Honglian CMS line of rice[J]. Plant Cell Reports, 26: 373-382. [34] Xu J, Ding Z W, Vizcay-Barrena G, et al. 2014. ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis[J]. The Plant Cell, 26: 1544-1556.
