Cytological abnormalities during pollen development in interspecific hybrids of Nicotiana
Jugou Liao A * , Jingwen Zhang A * , Xuemei Wei A , Yongzhi Niu B , Wenlong Suo B , Yunye Zheng C , Wenguang Ma C and Suiyun Chen
A D
+ Author Affiliations
- Author Affiliations
A School of Ecology and Environmental Sciences, Biocontrol Engineering Research Center of Plant Diseases & Pests, Biocontrol Engineering Research Center of Crop Diseases & Pests, Yunnan University, Kunming, Yunnan 650091, China.
B Yuxi China Tobacco Seed Company Ltd, Yuxi, Yunnan 653100, China.
C Yunnan Academy of Tobacco Agricultural Sciences, Yuxi, Yunnan 653100, China.
D Corresponding author. Email: chensuiyun@ynu.edu.cn
Crop and Pasture Science 71(12) 1029-1040 https://doi.org/10.1071/CP20155
Submitted: 9 May 2020 Accepted: 29 September 2020 Published: 8 December 2020
Abstract
Nicotiana alata is resistant to Tomato spotted wilt virus (TSWV) and of great value in breeding. However, hybrid sterility constrains the application of interspecific genetic resources. Previously, we obtained interspecific hybrids between a cytoplasmic male sterility (CMS) line of Nicotiana tabacum and N. alata, some of which were pollen sterile. In the present research, we studied the cytological abnormalities during pollen development in sterile hybrids (F1-D) by comparing pollen development with that in fertile hybrids (F1-S) from the same cross. Transmission electron microscopy and DiI staining showed that the membrane structures of microspores and pollen in F1-D sterile hybrids were impaired. Carbol fuchsin staining revealed that cytomixis, chromosome loss and asymmetric callose wall formation occurred with high frequency in the microsporocytes and microspores of the sterile hybrids. The cytoplasm and nucleus were lost in the microspores and pollen of sterile hybrids, leading to mature pollen grains that were vacuous and collapsed in the aperture region. In addition, delayed tapetum degradation was detected in the anther of sterile hybrids, and sporopollenin was deposited in the aperture region. Impaired membrane structures of microspores and pollen in F1-D sterile hybrids affected the integrity of the cells, and might be associated with chromosome, nuclear and cytoplasm loss, vacuous pollen, and sterility in F1-D hybrids. Abnormal tapetum degradation in the anther and irregular sporopollenin deposition in the pollen wall of the F1-D sterile hybrids might also be related to the pollen sterility. This study deepens our understanding of the cytological mechanisms of hybrid sterility, and may facilitate the application of TSWV-resistant resources in cultivated Nicotiana species through hybrid fertility restoration and backcross breeding.
Keywords: abnormal cell structures, interspecific hybrids, Nicotiana, pollen sterility, tapetum degradation, vacuous pollen grains.
References
Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annual Review of Plant Biology 62, 437–460.| Genetic regulation of sporopollenin synthesis and pollen exine development.Crossref | GoogleScholarGoogle Scholar | 21275644PubMed |
Basavaiah D, Murthy TCS (1987) Cytomixis in pollen mother cells of Urochloa panicoides P. Beauv. (Poaceae). Cytologia 52, 69–74.
| Cytomixis in pollen mother cells of Urochloa panicoides P. Beauv. (Poaceae).Crossref | GoogleScholarGoogle Scholar |
Bharaj TS, Virmani SS, Khush GS (1995) Chromosomal location of fertility restoring genes for ‘wild abortive’ cytoplasmic male sterility using primary trisomics in rice. Euphytica 83, 169–173.
| Chromosomal location of fertility restoring genes for ‘wild abortive’ cytoplasmic male sterility using primary trisomics in rice.Crossref | GoogleScholarGoogle Scholar |
Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytologist 174, 483–498.
| Pollen wall development in flowering plants.Crossref | GoogleScholarGoogle Scholar | 17447905PubMed |
Caetano-Pereira C, Pagliarini MS (1997) Cytomixis in maize microsporocytes. Cytologia 62, 351–355.
| Cytomixis in maize microsporocytes.Crossref | GoogleScholarGoogle Scholar |
Carrizo Garcia C (2002) Anther wall formation in Solanaceae species. Annals of Botany 90, 701–706.
| Anther wall formation in Solanaceae species.Crossref | GoogleScholarGoogle Scholar | 12451025PubMed |
Dong XY, Hong ZL, Sivaramakrishnan M, Mahfouz M, Verma DPS (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. The Plant Journal 42, 315–328.
| Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Falasca G, D’Angeli S, Biasi R, Fattorini L, Matteucci M, Canini A, Altamura MM (2013) Tapetum and middle layer control male fertility in Actinidia deliciosa. Annals of Botany 112, 1045–1055.
| Tapetum and middle layer control male fertility in Actinidia deliciosa.Crossref | GoogleScholarGoogle Scholar | 23965617PubMed |
FeijÓ JA, Pais MSS (1989) Cytomixis in meiosis during the microsporogenesis of Ophris lutea: an ultrastructural study. Caryologia 42, 37–48.
| Cytomixis in meiosis during the microsporogenesis of Ophris lutea: an ultrastructural study.Crossref | GoogleScholarGoogle Scholar |
Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. The Plant Cell 5, 1217–1229.
Fernández Gómez JF, Wilson ZA (2014) A barley PHD finger transcription factor that confers male sterility by affecting tapetal development. Plant Biotechnology Journal 12, 765–777.
| A barley PHD finger transcription factor that confers male sterility by affecting tapetal development.Crossref | GoogleScholarGoogle Scholar |
Fernández Gómez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. Journal of Integrative Plant Biology 57, 876–891.
| Anther and pollen development: a conserved developmental pathway.Crossref | GoogleScholarGoogle Scholar |
Haque SM, Ghosh B (2017) Cell division study in pollen mother cells and pollen grains of in vivo and ex vitro plants in Drimiopsis botryoides. Grana 56, 124–136.
| Cell division study in pollen mother cells and pollen grains of in vivo and ex vitro plants in Drimiopsis botryoides.Crossref | GoogleScholarGoogle Scholar |
He JH, Shahid MQ, Li YJ, Guo HB, Cheng XA, Liu XD, Lu YG (2011) Allelic interaction of F-1 pollen sterility loci and abnormal chromosome behavior caused pollen sterility in intersubspecific autotetraploid rice hybrids. Journal of Experimental Botany 62, 4433–4445.
| Allelic interaction of F-1 pollen sterility loci and abnormal chromosome behavior caused pollen sterility in intersubspecific autotetraploid rice hybrids.Crossref | GoogleScholarGoogle Scholar | 21624978PubMed |
Junqueira VB, Costa AC, Boff T, Mueller C, Correa Mendonca MA, Batista PF (2017) Pollen viability, physiology, and production of maize plants exposed to pyraclostrobin plus epoxiconazole. Pesticide Biochemistry and Physiology 137, 42–48.
| Pollen viability, physiology, and production of maize plants exposed to pyraclostrobin plus epoxiconazole.Crossref | GoogleScholarGoogle Scholar | 28364803PubMed |
Kamra OP (1960) Chromatin extrusion and cytomixis in pollen mother cells of Hordeum. Hereditas 46, 592–600.
| Chromatin extrusion and cytomixis in pollen mother cells of Hordeum.Crossref | GoogleScholarGoogle Scholar |
Kravets EA (2013) Cytomixis and its role in the regulation of plant fertility. Russian Journal of Developmental Biology 44, 113–128.
| Cytomixis and its role in the regulation of plant fertility.Crossref | GoogleScholarGoogle Scholar |
Larson DA, Skvarla JJ (1996) Fine structural studies of Zea mays pollen: cell membranes and exine ontogeny. American Journal of Botany 53, 1112–1125.
Laskowska D, Doroszewska T, Depta A, Kursa K, Olszak-Przybys H, Czubacka A (2013) A survey of Nicotiana germplasm for resistance to Tomato spotted wilt virus (TSWV). Euphytica 193, 207–219.
| A survey of Nicotiana germplasm for resistance to Tomato spotted wilt virus (TSWV).Crossref | GoogleScholarGoogle Scholar |
Liao JG, Dai JR, Yang SY, Zhou XL, Ren LH, Chen ZZ, He HL, Chen SY (2017) Interspecific cross-hybrids of Nicotiana tabacum L. cv. (gla.) S ‘K326’ with Nicotiana alata. Plant Breeding 136, 427–435.
| Interspecific cross-hybrids of Nicotiana tabacum L. cv. (gla.) S ‘K326’ with Nicotiana alata.Crossref | GoogleScholarGoogle Scholar |
Chen L,, Liu YG (2014) Male sterility and fertility restoration in crops. Annual Review of Plant Biology 65, 579–606.
| Male sterility and fertility restoration in crops.Crossref | GoogleScholarGoogle Scholar |
Long YM, Zhao LF, Niu BX, Su J, Wu H, Chen YL, Zhang QY, Guo JX, Zhuang CX, Mei MT, Xia JX, Wang L, Wu HB, Liu YG (2008) Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proceedings of the National Academy of Sciences of the United States of America 105, 18871–18876.
| Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes.Crossref | GoogleScholarGoogle Scholar |
Lu P, Chai M, Yang J, Ning G, Wang G, Ma H (2014) The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 gene is required for male fertility through regulating callose metabolism during microsporogenesis. Plant Physiology 164, 1893–1904.
| The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 gene is required for male fertility through regulating callose metabolism during microsporogenesis.Crossref | GoogleScholarGoogle Scholar | 24567187PubMed |
Luo JR, Van Tuyl JM, Arens P, Niu LX (2013) Cytogenetic studies on meiotic chromosome behaviors in sterile Oriental × Trumpet lily. Genetics and Molecular Research 12, 6673–6684.
| Cytogenetic studies on meiotic chromosome behaviors in sterile Oriental × Trumpet lily.Crossref | GoogleScholarGoogle Scholar | 24391009PubMed |
Maheshwari S, Barbash DA (2011) The genetics of hybrid incompatibilities. Annual Review of Genetics 45, 331–355.
| The genetics of hybrid incompatibilities.Crossref | GoogleScholarGoogle Scholar | 21910629PubMed |
Mallick EH (1980) Induced cytoplasmic male sterility and fertility restoration and production of hybrid rice. Genetica Agraria 34, 207–213.
Miedaner T, Herter CP, Gosslau H, Wilde P, Hackauf B (2017) Correlated effects of exotic pollen-fertility restorer genes on agronomic and quality traits of hybrid rye. Plant Breeding 136, 224–229.
| Correlated effects of exotic pollen-fertility restorer genes on agronomic and quality traits of hybrid rye.Crossref | GoogleScholarGoogle Scholar |
Moyle LC, Nakazato T (2008) Comparative genetics of hybrid incompatibility: sterility in two Solanum species crosses. Genetics 179, 1437–1453.
| Comparative genetics of hybrid incompatibility: sterility in two Solanum species crosses.Crossref | GoogleScholarGoogle Scholar | 18562656PubMed |
Mursalimov S, Sidorchuk Y, Deineko E (2017) Behavior of nucleolus in the tobacco male meiocytes involved in cytomixis. Cell Biology International 41, 340–344.
| Behavior of nucleolus in the tobacco male meiocytes involved in cytomixis.Crossref | GoogleScholarGoogle Scholar | 28032378PubMed |
Mwathi MW, Gupta M, Atri C, Banga SS, Batley J, Mason AS (2017) Segregation for fertility and meiotic stability in novel Brassica allohexaploids. Theoretical and Applied Genetics 130, 767–776.
| Segregation for fertility and meiotic stability in novel Brassica allohexaploids.Crossref | GoogleScholarGoogle Scholar | 28097399PubMed |
Nikova V, Vladova R, Pundeva R (1997) Cytoplasmic male sterility in Nicotiana tabacum L. obtained through interspecific hybridization. Euphytica 94, 375–378.
| Cytoplasmic male sterility in Nicotiana tabacum L. obtained through interspecific hybridization.Crossref | GoogleScholarGoogle Scholar |
Novo PE, Valls JFM, Galdeano F (2016) Interspecific hybrids between Paspalum plicatulum and P. oteroi: a key tool for forage breeding. Crop Science 73, 356–362.
Okada H, Hambali G (1989) Chromosome behaviors in meiosis of the inter-specific hybrids between Colocasia esculenta (L.) Schott and Colocasia gigantea Hook f. Cytologia 54, 389–393.
| Chromosome behaviors in meiosis of the inter-specific hybrids between Colocasia esculenta (L.) Schott and Colocasia gigantea Hook f.Crossref | GoogleScholarGoogle Scholar |
Onyemaobi I, Liu H, Siddique KHM, Yan G (2017) Both male and female malfunction contributes to yield reduction under water stress during meiosis in bread wheat. Frontiers in Plant Science 7, 2071
| Both male and female malfunction contributes to yield reduction under water stress during meiosis in bread wheat.Crossref | GoogleScholarGoogle Scholar | 28119733PubMed |
Pacini E, Franchi GG, Hesse M (1985) The tapetum: its form, function, and possible phylogeny in Embryophyta. Plant Systematics and Evolution 149, 155–185.
| The tapetum: its form, function, and possible phylogeny in Embryophyta.Crossref | GoogleScholarGoogle Scholar |
Pierozzi NI, Moura MF (2014) Cytological analyses in ‘Niagara Branca’ grape and in its somatic mutant ‘Niagara Rosada’. Notulae Botanicae Horti Agrobota 42, 460–465.
| Cytological analyses in ‘Niagara Branca’ grape and in its somatic mutant ‘Niagara Rosada’.Crossref | GoogleScholarGoogle Scholar |
Scott RJ, Speilman M, Dickinson HG (2004) Stamen structure and function. The Plant Cell 16, S46–S60.
| Stamen structure and function.Crossref | GoogleScholarGoogle Scholar | 15131249PubMed |
Shi X, Sun XH, Zhang ZG, Feng D, Zhang Q, Han LD, Wu JX, Lu TG (2015) Glucan synthase-like 5 (GSL5) plays an essential role in male fertility by regulating callose metabolism during microsporogenesis in rice. Plant & Cell Physiology 56, 497–509.
| Glucan synthase-like 5 (GSL5) plays an essential role in male fertility by regulating callose metabolism during microsporogenesis in rice.Crossref | GoogleScholarGoogle Scholar |
Sidorchuk YV, Deineko EV, Shumnyi VK (2004) Cytomixis in mother pollen cells of transgenic tobacco (Nicotiana tabacum L.) plants. Doklady Biological Sciences 394, 47–50.
| Cytomixis in mother pollen cells of transgenic tobacco (Nicotiana tabacum L.) plants.Crossref | GoogleScholarGoogle Scholar | 15088403PubMed |
Sidorchuk IuV, Deineko EV, Shumnyi VK (2007) The role of microtubular cytoskeleton and callose walls in the cytomixis process in tobacco (Nicotiana tabacum L.) pollen mother cells. Tsitologiia 49, 876–880.
Simon M, Durand S, Pluta N, Gobron N, Botran L, Ricou A, Camilleri C, Budar F (2016) Genomic conflicts that cause pollen mortality and raise reproductive barriers in Arabidopsis thaliana. Genetics 203, 1353–1367.
| Genomic conflicts that cause pollen mortality and raise reproductive barriers in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 27182945PubMed |
Soares TL, Souza EH de, Costa MAPC, Silva SO e, Santos-Serejo JA dos (2016) Viability of pollen grains of tetraploid banana. Bragantia 75, 145–151.
| Viability of pollen grains of tetraploid banana.Crossref | GoogleScholarGoogle Scholar |
Tanaka M, Ishii H (1975) Hybrid sterility and chromosomal interchanges found in the Timopheevi group of tetraploid wheat. Japanese Journal of Genetics 50, 141–149.
| Hybrid sterility and chromosomal interchanges found in the Timopheevi group of tetraploid wheat.Crossref | GoogleScholarGoogle Scholar |
Wang J, You HL, Tian J, Wang YF, Liu MH, Duan WL (2015) Abnormal meiotic chromosome behavior and gametic variation induced by intersectional hybridization in Populus L. Tree Genetics & Genomes 11, 61
| Abnormal meiotic chromosome behavior and gametic variation induced by intersectional hybridization in Populus L.Crossref | GoogleScholarGoogle Scholar |
Waterkeyn L (1962) Les parois microsporocytaires de nature callosique chez Helleborus et Tradescantia. La Cellule 62, 225–255.
Waterkeyn L, Bienfait A (1970) On a possible function of the callosic special wall in Ipomoea purpurea (L) Roth. Grana 10, 13–20.
| On a possible function of the callosic special wall in Ipomoea purpurea (L) Roth.Crossref | GoogleScholarGoogle Scholar |
Xie B, Deng Y, Kanaoka MM, Okada K, Hong Z (2012) Expression of Arabidopsis callose synthase 5 results in callose accumulation and cell wall permeability alteration. Plant Science 183, 1–8.
| Expression of Arabidopsis callose synthase 5 results in callose accumulation and cell wall permeability alteration.Crossref | GoogleScholarGoogle Scholar | 22195570PubMed |
Xu J, Ding Z, Vizcay-Barrena G (2014) Aborted microspores acts as a master regulator of pollen wall formation in Arabidopsis. The Plant Cell 26, 1544–1556.
| Aborted microspores acts as a master regulator of pollen wall formation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24781116PubMed |
Yang Y-X, Li YH, Tong JF, Qasim SM, Chen ZX, Wang L, Li JQ, Liu XD, Lu YG (2012) Wide-compatibility gene S5n exploited by functional molecular markers and its effect on fertility of intersubspecific rice hybrids. Crop Science 52, 669–675.
| Wide-compatibility gene S5n exploited by functional molecular markers and its effect on fertility of intersubspecific rice hybrids.Crossref | GoogleScholarGoogle Scholar |
Yang Z, Liu L, Sun L, Yu P, Zhang PP, Abbas A, Xiang XJ, Wu WX, Zhang YX, Cao LY, Cheng SH (2019) OsMS1 functions as a transcriptional activator to regulate programmed tapetum development and pollen exine formation in rice. Plant Molecular Biology 99, 175–191.
| OsMS1 functions as a transcriptional activator to regulate programmed tapetum development and pollen exine formation in rice.Crossref | GoogleScholarGoogle Scholar | 30610522PubMed |
Zadoo SN, Choubey RN, Gupta SK, Premachandran MN (1988) Chromosomal stability in the backcross progenies of pentaploid hybrids between Avena sativa L. and A. maroccana Gdgr. Plant Breeding 100, 316–319.
| Chromosomal stability in the backcross progenies of pentaploid hybrids between Avena sativa L. and A. maroccana Gdgr.Crossref | GoogleScholarGoogle Scholar |
Zhang ZS, Lu YG, Liu XD, Feng JH, Zhang GQ (2006) Cytological mechanism of pollen abortion resulting from allelic interaction of F-1 pollen sterility locus in rice (Oryza sativa L.). Genetica 127, 295–302.
| Cytological mechanism of pollen abortion resulting from allelic interaction of F-1 pollen sterility locus in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 16850233PubMed |
Zhang D, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. Journal of Genetics and Genomics 38, 379–390.
| Cytological analysis and genetic control of rice anther development.Crossref | GoogleScholarGoogle Scholar | 21930097PubMed |
Zhao ZG, Jiang L, Zhang WW, Yu CY, Zhu SS, Xie K, Tian H, Liu LL, Ikehashi H, Wan JM (2007) Fine mapping of S31, a gene responsible for hybrid embryo-sac abortion in rice (Oryza sativa L.). Planta 226, 1087–1096.
| Fine mapping of S31, a gene responsible for hybrid embryo-sac abortion in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 17549514PubMed |
Zhao B, Shi H, Wang W, Liu X, Gao H, Wang X, Zhang Y, Yang M, Li R, Guo Y (2016) Secretory CopII protein SEC31B is required for pollen wall development. Plant Physiology 172, 1625–1642.
| Secretory CopII protein SEC31B is required for pollen wall development.Crossref | GoogleScholarGoogle Scholar | 27634427PubMed |
