Scientia Agricultura Sinica ›› 2015, Vol. 48 ›› Issue (14): 2687-2696.doi: 10.3864/j.issn.0578-1752.2015.14.001

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS •     Next Articles

Organization Changes of Actin Cytoskeleton and Callose with the Expression Analysis of Related Genes in Physiological Male Sterile Wheat

ZHANG Jiao1, ZHU Qi-di1,2, JU Lan1, ZHANG Gai-sheng1, YU Yong-ang1, NIU Na1, WANG Jun-wei1, MA Shou-cai1   

  1. 1College of Agronomy, Northwest A&F University /National Yangling Agricultural Biotechnology & Breeding Center /Yangling Branch of State Wheat Improvement Centre /Wheat Breeding Engineering Research Center, Ministry of Education /Key Laboratory of Crop Heterosis of Shaanxi Province, Yangling 712100, Shaanxi
    2College of Life Science and Technology, Henan College of Science and Technology, Xinxiang 453003, Henan
  • Received:2015-01-12 Online:2015-07-16 Published:2015-07-16

Abstract: 【Objective】The organization of actin filaments and callose and the expression of related genes in physiological male sterility wheat pollen cells were studied to reveal the relationship between actin filaments and callose and pollen abortion in physiological male sterility wheat. The results of the study will provide a theoretical basis for further study on the mechanism of male sterility induced by chemical hybridizing agents SQ-1 in wheat. 【Method】The physiological male sterility line ms(A)-Xinong1376 and corresponding normal fertile wheat (A)-xinong1376 were used as test materials. The TRITC-phalloidin was used to stain actin filaments and Aniline blue was used to stain callose. QRT-PCR was used to analyze the expression of TaADF (Actin depolymerizing factor) and TaGSL (Glucan synthase-like).【Result】At prophase I, metaphase I, and anaphase I, there were no significant differences between physiological male sterility and male fertility. At prophase I, actin filaments distributed in cytoplasm of the cell and there was also distribution of some actin filaments in nuclear zone. At metaphase I, actin filaments distributed in cytoplasm. They were stained deeper in the spindle position and formed actin spindle. At anaphase I, actin filaments between the poles of the chromosomes were stained deeper, so there were more actin filaments distributed there. At early telophase I, we observed that there were no sharp actin filaments at leading edges of phragmoplasts and the overlapped actin filaments at midline were obscure in physiological male sterility. At late telophase I, there was a cell plate at the midline of phragmoplasts, it was linear and smooth, but in the physiological male sterile line, the linear cell plate was not seen, the midzone of dyads was hollow. At the same time, the deposition of callose on the cell plate was insufficient and the cell plate was wrinkled and cleft. At tetrad, actin filaments were obscure and had no silky feeling and callose fluorescence was weaker in the physiological male sterile. Then qRT-PCR technique was performed to analyze the expression patterns of the TaADF gene and TaGSL gene in sterile and fertile anthers during meiosis. The results indicated that the transcript of TaADF in the treated anthers was 4.28 times higher than that of the control. It indicated that because of the increased expression of TaADF, the rate of dissociation of actin filaments was increased, so the microfilaments were obscure. The transcript of TaGSL in the treated anthers was 0.83 times lower than that of the control. Callose deposition was influenced by SQ-1. 【Conclusion】The increased expression level of TaADF in the physiological male sterility line destroyed the normal structure of actin filaments. The actin filaments could not execute their functions. Then it may influence certain metabolic pathways associated with fertility in anther development. At the same time, abnormal actin filaments caused abnormal cell plate formation which may have an effect on callose deposition. Therefore, it was estimated that it has a close relationship among the changes of actin filaments and callose and the physiological male sterility induced by SQ-1.

Key words: common wheat, physiological male sterile, meiosis, actin filaments, callose

[1]    位明明, 王俊生, 张改生, 张龙雨, 袁正杰, 孙瑞, 叶景秀, 牛娜, 马守才, 李红霞. GAPDH基因表达与小麦生理型雄性不育花药败育的关系. 分子植物育种, 2009, 27(4): 679-684.
Wei M M, Wang J S, Zhang G S, Zhang L Y, Yuan Z J, Sun R, Ye J X, Niu N, Ma S C, Li H X. Relationship between the expression of GAPDH gene and anther abortion of physiological male sterile of wheat. Molecular Plant Breeding, 2009, 27(4): 679-684. (in Chinese)
[2]    朱启迪, 桑青, 王春平, 张改生, 陈征, 赵新亮, 马守才, 王军卫, 牛娜. 高效液相色谱法测定小麦籽粒中杀雄嗪酸残留. 分析化学, 2013, 41(4): 565-569.
Zhu Q D, Sang Q, Wang C P, Zhang G S, Chen Z, Zhao X L, Ma S C, Wang J W, Niu N. Determination of clofencet in wheat grain by high performance liquid chromatography. Chinese Journal of Analytical Chemistry, 2013, 41(4): 565-569. (in Chinese)
[3]    刘宏伟, 张改生, 刘秉华. 化学杂交剂GENESIS诱导小麦雄性不育的细胞形态学观察. 西北植物学报, 2004, 24(12): 2282-2285.
Liu H W, Zhang G S, Liu B H. Cytological observations on male sterile anther and pollen developments induced by chemical hybridizing agent GENESIS in wheat. Acta Botanica Boreali- Occidentalia Sinica, 24(12): 2282-2285. (in Chinese)
[4]    盛英, 张改生, 李亚鑫, 张龙雨, 王书平, 赵新亮, 王亮明, 宋瑜龙. 小麦生理型雄性不育花药绒毡层和孢粉素变化与RAFTIN1表达的关系. 中国农业科学, 2011, 44(19): 3937-3944.
Sheng Y, Zhang G S, Li Y X, Zhang L Y, Wang S P, Zhao X L, Wang L M, Song Y L. The relationship on anther tapetum, sporopollenin and expression of RAFTIN1 in physiological male sterile wheat. (in Chinese)Scientia Agricultura Sinica, 2011, 44(19): 3937-3944.
[5]    张龙雨, 袁蕾, 杨书玲, 张改生, 王俊生, 宋瑜龙, 赵卓军, 牛娜, 马守才. 小麦雄性不育系中TaPDC-E1α及其调节酶基因的表达特征. 作物学报, 2011, 37(4): 620-628.
Zhang L Y, Yuan L, Yang S L, Zhang G S, Wang J S, Song Y L, Zhao Z J, Niu N, Ma S C. Expression characteristic on TaPDC-E1α gene and its regulatory enzymes gene in male sterile line of wheat (Triticum aestivum). Acta Agronomica Sinica, 2011, 37(4): 620-628. (in Chinese)
[6]    巴青松, 张改生, 车会学, 刘红占, 张龙雨, 王书平. 小麦生理型雄性不育系中反式烯脂酰-CoA还原酶基因(TaECR)的克隆及表达分析. 农业生物技术学报, 2013, 21(7): 792-798.
Ba Q S, Zhang G S, Che H X, Liu H Z, Zhang L Y, Wang S P. Cloning and expression characteristic of trans-2,3-enoyl-coA reductase gene (TaECR) in physiological male sterile line of wheat(Triticum aestivura). Journal of Agricultural Biotechnology, 2013, 21(7): 792-798. (in Chinese)
[7]    Xu S X, Liu X D, Feng J H, Lu Y G. Comparative studies on the changes of microtubule distribution and reorganization during the meiotic stages of development in normal (IR36) and a temperature/ photoperiod sensitive male sterile line (Peiai 64s) of rice. Acta Botanica Sinica, 2001, 43(3): 221-226.
[8]    Ye X L, Yeung E, Xu S X, Liang C Y. Microtubule structure and male sterility in a gene-cytoplasmic male sterile line of rice Zhen Shan 97A. Acta Botanica Sinica, 2003, 45(2): 183-192.
[9]    姚雅琴, 李蓓, 张英利, 牛娜, 张改生. 细胞骨架与小麦雄性不育关系研究初报. 西北农林科技大学学报: 自然科学版, 2005, 33(12): 39-42.
Yao Y Q, Li B, Zhang Y L, Niu N, Zhang G S. Preliminary studies on relationship between the cytoskeleton and the male sterile lines of wheat. Journal of Northwest A&F University: Nature Science Edition, 2005, 33(12): 39-42. (in Chinese)
[10]   Dong C H, Xia G X, Hong Y, Ramachandran S, Kost B, Chua N H. ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. The Plant Cell, 2001, 13(6): 1333-1346.
[11]   Chen C Y, Wong E I, Vidali L, Estavillo A, Hepler P K, Wu H M, Cheung A Y. The regulation of actin organization by actin-depolymorizing factor in elongating pollen tubes. The Plant Cell, 2002, 14(9): 2175-2190.
[12]   Nishikawa S, Zinkl G M, Swanson R J, Maruyama D, Preuss D. Callose (β-1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biology, 2005, 5: 22-30.
[13]   张文超, 曹媛, 常童洁, 荆艳萍. 毛白杨花粉败育过程中胼胝质的异常分布变化. 东北林业大学学报, 2013, 41(1): 68-71.
Zhang W C, Cao Y, Chang T J, Jing Y P. Abnormal changes of callose distribution during pollen abortion in populus tomentosa Carr. Journal of Northeast Forestry University, 2013, 41(1): 68-71. (in Chinese)
[14]   Dong X Y, Hong Z L, Sivaramakrishnan M S, Mahfouz M, Verma D P S. Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. The Plant Journal, 2005, 42(3): 315-328.
[15]   Chen R, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, Zhao J, Sun M, He R, He G. Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genie male sterility. The Plant Cell, 2007, 3: 847-861.
[16]   Livak K J, Schmittgen T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△Ct method. Methods, 2001, 25(4): 402-408.
[17]   Voigt C A, Schafer W, Salomon S. A comprehensive view on organ-specific callose synthesis in wheat (Triticum aestivum L.): glucan synthase-like gene expression, callose synthase activity, callose quantification and deposition. Plant Physiology and Biochemistry, 2006, 44: 242-247.
[18]   Wasteneys G O, Yang Z B. New views on the plant cytoskeleton. Plant Physiology, 2004, 136(4): 3884-3891.
[19]   Hussey P J, Ketelaar T, Deeks M J. Control of the actin cytoskeleton in plant cell growth. Annual Review of Plant Biology, 2006, 57: 109-125.
[20]   Higaki T, Kutsuna N, Sano T, Hasezawa S. Quantitative analysis of changes in actin microfilament contribution to cell plate development in plant cytokinesis. BMC Plant Biology, 2008, 8: 80-85.
[21]   Xu S X, Wang L J, Qiu Z P, Ye Y J, Yu X H. Actin visualization in living immature pollen of rice using a GFP-mouse talin fusion protein. Acta Botanica Sinica, 2002, 44(6): 642-648.
[22]   Xu S X, Ye X L, Wang L J, Qiu Z P, Ye Y J. Factin visualization in generative and sperm cells of living pollen of rice using a GFP-mouse talin fusion protein. Acta Botanica Sinica, 2003, 45(8): 949-958.
[23]   许晨光, 刘泽涛, 苑少华, 张立平, 赵昌平, 张胜全, 张风廷. 不同固定液对小麦花粉母细胞微丝骨架荧光标记的效果. 作物杂志, 2012, 4: 13-16.
Xu C G, Liu Z T, Yuan S H, Zhang L P, Zhao C P, Zhang S Q, Zhang F T. Results of fluorescent labeling of actin cytoskeleton in pollen mother cell of wheat fixed by different fixatives. Crops, 2012, 4: 13-16. (in Chinese)
[24]   Cleary A L, Gunning B E S, Wasteneys G O, Hepler P K. Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells. Journal of Cell Science, 1992, 103(12): 977-988.
[25]   Yoneda A, Kutsuna N, Higaki T, Oda Y, Sano T, Hasezawa S. Recent progress in living cell imaging of plant cytoskeleton and vacuole using fluorescent-protein transgenic lines and three-dimensional imaging. Protoplasma, 2007, 230: 129-139.
[26]   Kitamura S, Akutsu M, Okazaki K. Mechanism of action of nitrous oxide gas applied as a polyploidizing agent during meiosis in lilies. Sexual Plant Reproduction, 2009, 22(1): 9-14.
[27]   Tchorzewska D, Bednara J. The dynamics of the actin cytoskeleton during sporogenesis in Psilotum nudum L.. Protoplasma, 2011, 248(2): 289-298.
[28]   Molchan T M, Valster A H, Hepler P K. Actomyosin promotes cell plate alignment and late lateral expansion in Tradescantia stamen hair cells. Planta, 2002, 214(5): 683-693.
[29]   Collings D A, Harper J D I, Vaughn K C. The association of peroxisomes with the developing cell plate in dividing onion root cells depends on actin microfilaments and myosin. Planta, 2003, 218(2): 204-216.
[30]   Jurgens G. Cytokinesis in higher plants. Annual Review of Plant Biology, 2005, 56: 281-299.
[31]   Staiger C J, Cande W Z. Microfilament distribution in maize meiotic mutants correlates with microtubule organization. The Plant Cell, 1991, 3(6): 637-644.
[32]   Xu C G, Liu Z T, Zhang L P, Zhao C P, Yuan S H, Zhang F T. Organization of actin cytoskeleton during meiosis I in a wheat thermo-sensitive genic male sterile line. Protoplasma, 2013, 250(1): 415-422.
[33]   Carlier M F, Laurent V, Santolini J, Melki R, Didry D, Xia G X, Hong Y, Chua N H, Pantaloni D. Actin depolymerizing factor (ADF/cofilin ) enhances the rate filament turnover: Implication in actin-based motility. The Journal of Cell Biology, 1997, 136(6): 1307-1322.
[34]   叶纨芝, 曹家树, 金维正. 植物胞质分裂发生机制. 细胞生物学杂志, 2005, 27: 313-318.
Ye W Z, Cao J S, Jin W Z. The mechanism of plant cytokinesis. Chinese Journal of Cell Biology, 2005, 27: 313-318. (in Chinese)
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