Cytochemical investigation at different microsporogenesis phases of male sterility in wheat, as induced by the chemical hybridising agent SQ-1
Yulong Song A , Junwei Wang A , Pengfei Zhang A , Gaisheng Zhang A B , Longyu Zhang A , Xinliang Zhao A , Na Niu A and Shoucai Ma A
+ Author Affiliations
- Author Affiliations
A Northwest A&F University, National Yangling Agricultural Biotechnology and 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, P.R. China.
B Corresponding author. Email: zhanggsh58@aliyun.com
Crop and Pasture Science 65(9) 868-877 https://doi.org/10.1071/CP14034
Submitted: 25 January 2014 Accepted: 8 July 2014 Published: 29 August 2014
Abstract
This study used semi-thin sectioning and cytochemistry to investigate the relationship between pollen nutrient metabolism and pollen abortion in male sterile lines of wheat induced by SQ-1 (a chemical hybridising agent). Anthers were collected from the tetrad to trinucleate stages, and 4ʹ,6-diamidino-2-phenylindole staining was used to visualise nuclei and confirm the development stage. Sudan Black B, periodic acid–Schiff, Coomassie Brilliant Blue, and toluidine blue were used to detect lipids, starch, proteins, and acidic polyanions, respectively. Semi-thin sectioning indicated that nutrient accumulation was much higher in the fertile line 1376 than in the sterile line 1376-PHYMS. Further, no lipids were found in the free microspore stage in the sterile line; however, at the late microspore stage, more proteins and acidic polyanions were found in the sterile line 1376-PHYMS pollen than in the fertile line 1376 pollen. From the binucleate to trinucleate pollen stages, the starch content was low and the intine considerably thinner in the pollen of the 1376-PHYMS line. SQ-1 probably hampered nutrient metabolism in the anthers, leading to decreased nutrient supply and abnormal intine formation, ultimately resulting in pollen abortion. A new mechanism for nutrient absorption, i.e. endocytosis of Ubisch bodies or orbicules by the intine through the germinal aperture, was revealed.
Additional keywords: Triticum aestivum L., physiological male sterility, cytochemistry.
References
Abramova LI, Avalkina NA, Golubeva EA, Pyzhenkova ZS, Golubovskaya IN (2003) Synthesis and deposition of callose in anthers and ovules of meiotic mutants of maize (Zea mays). Russian Journal of Plant Physiology 50, 324–329.| Synthesis and deposition of callose in anthers and ovules of meiotic mutants of maize (Zea mays).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFyisbg%3D&md5=513885f3bf5902de183a01f0dd90b0c9CAS |
Chen CS, Lu YF, Zhang GS, Zhang ZJ, Li P, Zhang BY (2004) The synthesis of genesis and the research of bioactive chemicals. Chinese Journal of Pesticides 43, 315–317. [in Chinese]
Datta R, Chourey PS, Pring DR, Tang HV (2001) Gene-expression analysis of sucrose-starch metabolism during pollen maturation in cytoplasmic male-sterile and fertile lines of sorghum. Sexual Plant Reproduction 14, 127–134.
| Gene-expression analysis of sucrose-starch metabolism during pollen maturation in cytoplasmic male-sterile and fertile lines of sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFSjsw%3D%3D&md5=f100d3cec21faa627d6aa8160c5eb546CAS |
Dawson J, Wilson ZAMG, Aarts M, Braithwaite AF, Briarty LG, Mulligan BJ (1993) Microspore and pollen development in six male-sterile mutant of Arabidopsis thaliana. Canadian Journal of Botany 71, 629–638.
| Microspore and pollen development in six male-sterile mutant of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Dennis JD (1998) Hybrid wheat seed production using Genesis hybridizing agent [A]. In ‘The Proceedings of 1st International Workshop on Hybrid Wheat [C]’. pp. 23–26. (China Agricultural University Press: Beijing)
El-Ghazaly YG, Jensen WA (1987) Development of wheat (Triticum aestivum) pollen. II. Histochemical differentiation of wall and Ubisch bodies during development. American Journal of Botany 74, 1396–1418.
| Development of wheat (Triticum aestivum) pollen. II. Histochemical differentiation of wall and Ubisch bodies during development.Crossref | GoogleScholarGoogle Scholar |
Elkonin LA, Tsvetova MI (2008) Genetic and cytological analyses of the male sterility mutation induced in a sorghum tissue culture with streptomycin. Russian Journal of Genetics 44, 575–583.
| Genetic and cytological analyses of the male sterility mutation induced in a sorghum tissue culture with streptomycin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlShsbY%3D&md5=ded8771d1fb73c0e7bde7fdd6f870e56CAS |
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. American Journal of Botany 55, 123–142.
| Plant microtechnique: some principles and new methods.Crossref | GoogleScholarGoogle Scholar |
Han MJ, Jung KH, Yi G, Lee DY, An G (2006) Rice immature pollen 1 (RIP1) is a regulator of late pollen development. Plant & Cell Physiology 47, 1457–1472.
| Rice immature pollen 1 (RIP1) is a regulator of late pollen development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWqsr%2FO&md5=b6db2ebb15fdfebf6a23fe05aaaaf48cCAS |
Hu SY, Xu LF (1990) A cytochemical technique for demonstration of lipid drops, starch and protein bodies in thick resin sections. Acta Botanica Sinica 32, 841–846.
Knox RB (1984) The pollen grain. In ‘Embryology of angiosperms’. (Ed. BM Johri) pp. 197–271. (Springer: Berlin)
Knox RB, Heslop-Harrison JL (1969) Cytochemical localization of enzymes in the wall of the pollen grain. Nature 223, 92–94.
| Cytochemical localization of enzymes in the wall of the pollen grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXks1Oqsb0%3D&md5=f5070488ac01eb78f162d6f53886864dCAS |
Knox RB, Heslop-Harrison JL (1971) Pollen-wall proteins: the fate of intine-held antigens on the stigma in compatible and incompatible pollinations of Phalaris tuberosa L. Journal of Cell Science 9, 239–251.
Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. The Plant Cell 18, 2999–3014.
| The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1CltQ%3D%3D&md5=8cd100a7d619b4ad1b5d98055f3468c6CAS | 17138695PubMed |
Li FT, Chen SM, Chen FD, Teng NJ, Fang WM, Zhang F, Deng YM (2010) Anther wall development, microsporogenesis and microgametogenesis in male fertile and sterile chrysanthemum (Chrysanthemum morifolium Ramat., Asteraceae). Scientia Horticulturae 126, 261–267.
| Anther wall development, microsporogenesis and microgametogenesis in male fertile and sterile chrysanthemum (Chrysanthemum morifolium Ramat., Asteraceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVymtbnM&md5=fa5f8aa19d9f14c7599cb825c4d4e55dCAS |
Li DX, Li G, Feng SW, Ru ZG (2013) Cytochemical observation of fertile and sterile anthers of thermo-sensitive genic male-sterile wheat. Acta Agronomica Sinica 39, 878–884. [in Chinese]
Liu HW, Zhang GS, Wang JW, Wang XL, Fang ZW (2003) Effect of male sterility on different wheat genotype induced by SQ-1. Journal of Northwest Sci-Tech University of Agriculture and Forestry 31, 15–18.
Liu HW, Zhang GS, Liu BH (2004) Cytological observations on male sterile anther and pollen developments induced by chemical hybridizing agent genesis in wheat. Acta Botany Boreal-Occident Sinica 12, 2282–2285. [in Chinese]
Lynette BF, Said HF, Michael B, Anna S, Toshiyuki M, David T (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. PLOS Genetics 5, 1–10.
McRae DH (1985) Advances in chemical hybridization. In ‘Plant breeding reviews’. Vol. 3. (Ed. J Janick) pp. 169?191. (John Wiley & Sons, Inc.: Hoboken, NJ, USA)
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue. Protoplasma 59, 368–373.
| Polychromatic staining of plant cell walls by toluidine blue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2MXmtVOmsw%3D%3D&md5=4af13f663bcef3a549db1457039dc649CAS |
Pearse AGE (1985) Histochemistry, theoretical and applied. In ‘Analytical technology’. Vol. 2. 4th edn (Churchill Livingstone: Edinburgh)
Peng YF, Wang YR (1991) Studies on starch and protein contents of HPGMR during pollen abortion. Acta Scientiarum Naturalium Universitatis Sunyatseni 4, 92–99.
Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sexual Plant Reproduction 11, 65–80.
| Biogenesis and function of the lipidic structures of pollen grains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkt1KjsL8%3D&md5=cf75c62eae02b0dfec66166e4bcb5a23CAS |
Regan S, Moffatt B (1990) Cytochemical analysis of pollen development in wild-type Arabidopsis and a male-sterile mutant. The Plant Cell 2, 877–889.
| Cytochemical analysis of pollen development in wild-type Arabidopsis and a male-sterile mutant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlvFSjsw%3D%3D&md5=d95ffe2dbb1e233ef824014c4e1b51ddCAS | 12354970PubMed |
Rowell PL, Miller DG (1971) Induction of male sterility in wheat with 2-chloroethylposphonic acid. Crop Science 11, 629–631.
| Induction of male sterility in wheat with 2-chloroethylposphonic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XitFyltA%3D%3D&md5=18a7c9e6235f13f3da542759991c703eCAS |
Schnurr JA, Storey KK, Jung HJ, Somers DA, Gronwald JW (2006) UDP-sugar pyrophosphorylase is essential for pollen development in Arabidopsis. Planta 224, 520–532.
| UDP-sugar pyrophosphorylase is essential for pollen development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnsl2isLg%3D&md5=f9867e0106196857cf189556853ac736CAS | 16557401PubMed |
Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. The Plant Cell 16, S46–S60.
| Stamen structure and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFWltL8%3D&md5=02d65360351db0fc464c3a3f9058baa0CAS | 15131249PubMed |
Sevil TKFD (2012) Cytochemistry of pollen development in Campsis radicans (L.) Seem. (Bignoniaceae). Plant Systematics and Evolution 10, 1–12.
Sheng Y, Zhang GS, Li YX, Zhang LY, Wang SP, Zhao XL, Wang LM, Song YL (2011) The relationship on anther tapetum, sporopollenin and expression of RAFTIN1 in physiological male sterile wheat. Scientia Agricultura Sinica 44, 3937–3944. [in Chinese]
Southworth D (1990) Exine biochemistry. In ‘Microspores: evolution and ontogeny’. (Eds S Blackmore, RB Knox) pp. 193–212. (Academic Press: London)
Wang SP, Zhang GS, Ye JX, Li L, Song YL, Wang LM, Dai JJ, Zhang LY, Niu N, Ma SC, Zhu JC (2010) Differential proteomics analysis of floret intact chloroplasts proteins in wheat physiological male sterile line induced by CHA-SQ-1. Chinese Journal of Biochemistry and Molecular Biology 26, 854–861. [in Chinese]
Wei MM, Wang JS, Zhang GS, Zhang LY, Yuan ZJ, Sun R, Ye JX, Niu N, Ma SC, Li HX (2009) Relationship between the expression of GAPDH gene and anther abortion of physiological male sterile of wheat. Molecular Plant Breeding 7, 679–684. [in Chinese]
Wiermann R, Gubatz S (1992) Pollen wall and sporopollenin. International Review of Cytology 140, 35–72.
| Pollen wall and sporopollenin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1GisLs%3D&md5=0a176119efb9fd50dc1170040ea4df0cCAS |
Xie CT, Yang YH, Qiu YL, Zhu XY, Tian HQ (2005) Cytochemical investigation of genic male-sterility in Chinese cabbage. Sexual Plant Reproduction 18, 75–80.
| Cytochemical investigation of genic male-sterility in Chinese cabbage.Crossref | GoogleScholarGoogle Scholar |
Ye JX, Zhang GS, Wang SP, Chen RH, Wang JS, Niu N, Ma SC, Li HX, Zhu JC (2009) Differential proteomic studies on pollen grain proteins of wheat male sterile line induced by chemical hybridizing agent SQ-1. Chinese Journal of Biochemistry and Molecular Biology 25, 949–957. [in Chinese]
Zha RM, Ling YH, Yang ZL, Zhao FM, Zhong BQ, Xie R, Sang XC, He GH (2008) Prediction of hybrid grain yield performances in Indica rice (Oryza sativa L.) with effect-increasing loci. Molecular Breeding 22, 467–476.
| Prediction of hybrid grain yield performances in Indica rice (Oryza sativa L.) with effect-increasing loci.Crossref | GoogleScholarGoogle Scholar |
Zhang AM, Wang DQ, Chen WY, Huang TC, Nie XL, Ling Y (2001) The application technique of chemical hybridizing agents BAU9403[J]. Acta Tritical Crops 21, 20–24.
Zhang GS, Liu HW, Wang JW (2003) New variety of hybrid wheat with high resistance, quality and yield. Agriculture of New Technology 4, 25–26. [in Chinese]
Zhang LY, Zhang GS, Zhao XL, Yang SL (2013) Screening and analysis of proteins interacting with TaPDK from physiological male sterility induced by CHA in wheat. Journal of Integrative Agriculture 12, 941–950.
| Screening and analysis of proteins interacting with TaPDK from physiological male sterility induced by CHA in wheat.Crossref | GoogleScholarGoogle Scholar |
Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. The Plant Journal 55, 266–277.
| Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptlals7o%3D&md5=16810881b4120c44b2cc1ed5f682a5a1CAS | 18397379PubMed |
