Analysis of the cytohistological phenotype of anthers in sunflower with ASI-AG3 in the context of the PET1 mytotype and the allelic genotype for the Rf1 gene
DOI:
https://doi.org/10.52673/18570461.24.1-72.03Keywords:
androsterility, sunflower, cytohistological phenotype, Fertility, GibberellinsAbstract
Microsporogenesis and male gametogenesis are processes that, although under tight morphogenetic control, can often be affected by deviations of internal or external stimuli causing androsterility. The article examines the cytohistological phenotypes of sunflower anthers with gibberellin induced androsterility in plants with different mitotype and allelic genotype for the Rf1 gene, in comparison with the cytohistological phenotypes of fertile and sterile anthers (ASC-PET1). The treatment with gibberellic acid (AG3, 0.01%) was carried out by spraying the inflorescence at the budding stage. Cytological samples and those with semi-thin anther sections were analysed by light microscopy. It was determined that the gametocidal effects induced by AG3 associated with degenerative and early apoptotic events in tapetum cells were more severe in plants with sterile cytoplasm and nuclear Rf1 genes compared to those with fertile cytoplasm and no fertility-restoring genes. In plants with ASC, the exogenous gibberellin stimulus does not cause any visible compensatory events of the sterile phenotype, on the contrary, the effects of microsporogenesis inhibition are more temporally advanced, with sporogenous and sporophytic tissue cells showing various lesions in the premeiosis. The general common and differentiation characteristics found at the androsteril phenotypes suggest interactions between orfH522 and Rf1 gene expression products of negative feedback type in untreated plants and positive feedback type in AG3-treated ones. The research is relevant in the context of elucidating the physiological regulatory processes of the sensitivity of male gametophyte development to various stress conditions, which prospectively makes possible regulatory intervention in plants with different androsterility/androfertility control systems.
References
1. Hakeem, K.R., Rehman, R.U., Tahir, I. Plant signaling. Understanding the molecular crosstalk. New Delhi: Springer, 2014. 355 p. https://doi.org/10.1007/978-81-322-1542-4
2. Ku, Y.S., Sintaha, M., Cheung, M.Y., Lam, H.M. Plant hormone signaling crosstalks between biotic and abiotic stress responses. In: Int. J. Mol. Sci., 2018, vol. 19(10), 1-35. https://doi.org/10.3390/ijms19103206
3. Tal, L., Anleu, Gil, M.X., Guercio, A.M., Shabek, N. Structural aspects of plant hormone signal perception and regulation by ubiquitin ligases. In: Plant Physiology, 2020, vol. 182(4), 1537-1544. https://doi.org/10.1104/pp.19.01282
4. Song, S., Qi, T., Huang, H., Xie, D. Regulation of stamen development by coordinated actions of jasmonate, auxin, and gibberellin in Arabidopsis. In: Molecular Plant, 2013, vol. 6, 1065-1073. https://doi.org/10.1093/mp/sst054
5. Gómez, J.F., Talle, B., Wilson, Z.A. Anther and pollen development: A conserved developmental pathway. In: Journal of Integrative Plant Biology, 2015, vol. 57, 876-891. https://doi.org/10.1111/jipb.12425
6. Bao, S., Hua, C., Shen, L., Yu, H. New insights into gibberellin signaling in regulating flowering in Arabidopsis. In: Journal of Integrative Plant Biology,2020, vol. 62, 118-131. https://doi.org/10.1111/jipb.12892
7. Bao, S., Hua, C., Huang, G. et al. Molecular basis of natural variation in photoperiodic flowering responses. In: Developmental Cell, 2019, vol. 50, 90-101. https://doi.org/10.1016/j.devcel.2019.05.018
8. Wang, H., Pan, J., Li, Y. et al. The DELLA‐CONSTANS transcription factor cascade integrates gibberellic acid and photoperiod signaling to regulate flowering. In: Plant Physiology, 2016, vol. 172, 479-488. https://doi.org/10.1104/pp.16.00891
9. Lee, J.E., Goretti, D., Neumann, M., et al. A gibberellin methyltransferase modulates the timing of floral transition at the Arabidopsis shoot meristem. In: Physiol Plantarum, 2020, vol. 170, 474-487. https://doi.org/10.1111/ppl.13146
10. Wang, Y.H., Irving, H.R. Developing a model of plant hormone interactions. In: Plant Signal Behav, 2011, vol. 6(4), 494-500. https://doi.org/10.4161/psb.6.4.14558
11. Hirano, K., Aya, K., Hobo, T., et al. Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. In: Plant Cell Physiol, 2008, vol. 49, 1429-1450. https://doi.org/10.1093/pcp/pcn123
12. Andrew, R.G., Plackett, A.R.G., Wilson, Z.A. Gibberellins and Plant Reproduction. Annual Plant Reviews book series online, vol 49, 2017. https://doi.org/10.1002/9781119210436.ch11
13. Griffiths, J., Murase, K., Rieu, I., et al. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. In: The Plant Cell, 2006, vol. 18, 3399-3414. https://doi.org/10.1105/tpc.106.047415
14. Davière, J.M., Achard, P. Gibberellin signaling in plants. Development, 2013, vol. 140, 1147-1151. https://doi.org/10.1242/dev.087650
15. Chen, L., Liu, Y.G. Male sterility and fertility restoration in crops. In: Annual review of Plant Biology, 2014, nr. 65, 579-606. https://doi.org/10.1146/annurev-arplant-050213-040119
16. Baghali, Z., Majd, A., Chehregani, A., Pourpak, Z. Cytotoxic effect of benzo(a)pyrene on development and protein pattern of sunflower pollen grains. In: Toxicological & Environmental Chemistry, 2011, vol. 93(4), 665-677. https://doi.org/10.1080/02772248.2011.560851
17. Tripathi, S.M., Mani, S. Ethrel Induced Male Sterility in Helianthus Annuus L. In: Int. J. Mendel, 2010, vol. 24(34), 131-132.
18. Sharma, K.D., Nayyar, H. Regulatory Networks in Pollen Development under Cold Stress. In: Front. Plant Sci., 2016, vol. 7:402, 1-13. https://doi.org/10.3389/fpls.2016.00402
19. De Storme, N., Geelen, D. The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. In; Plant Cell Environ, 2014, vol. 37(1), 1-18. https://doi.org/10.1111/pce.12142
20. Balk, J., Leaver, C. J. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. In: The Plant Cell, 2001, vol. 13, 1803-1818. https://doi.org/10.1105/TPC.010116
21. Vianello, A., Zancani, M., Peresson, C. et al. Plant mitochondrial pathway leading to programmed cell death. In: Physiologia Plantarum, 2007, vol. 129, 242-252. https://doi.org/10.1111/j.1399-3054.2006.00767.x
22. Sabar, M., Gagliardi, D., Balk, J., Leaver, C., J. ORFB is a subunit of F1FO-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. In: EMBO reports, 2003, vol. 4, 381-386. https://doi.org/10.1038/sj.embor.embor800
23. Duca, M., Port, A., Midoni, A. ș.a. Moștenirea genelor Rf la diverse genotipuri de floarea-soarelui. În: Studia Universitatis. Ştiinţe ale Naturii, 2010, nr. 1, 5-9.
24. Port, A., Duca, M. Aspecte de semnalizare și expresie genică la plante. Universitatea de Stat "Dimitrie Cantemir˝, Centrul Genetică Funcțională. Chișinău: S. n., Tipografia Foxtrot, 2020. 194 p.
25. Schneiter, A., Miller, J.F. Description of Sunflower Growth Stages. In: Crop Science, 1981, vol. 21, 901-903. https://doi.org/10.2135/cropsci1981.0011183X002100060024x
26. Duca, M., Port, A., Nechifor, V. Corelarea dimensiunii florilor tubulare şi anterelor cu fazele microsporogenei şi microgametogenezei la Helianthus annuus L. În: "Agricultura modernă - realizări şi perspective". Materialele Simpozionului ştiinţific internaţional. Lucrări ştiinţifice UASM. Chișinău, 2013, vol. 39, 59-63.
27. Duca, M., Nechifor, V., Port, A. Profilul citologic al diviziunilor meiotice la plantele de floarea-soarelui cu androsterilitate indusă de gibereline. În: Buletinul Academiei de Ştiinţe a Moldovei. Ştiinţele Vieţii, 2017, nr. 3(333), 106-114.
28. Arisha, S.H. Biotechnology procedures and experiments handbook. Infinity science press llc hingham. Massachusetts. New Delhi, India, 2007. 710 p.
29. Weakley, B. A beginner's handbook in biological transmission electron microscopy. Churchill Livingstone, 1981, second ed. 252 p.
30. Horner, H.T. A comparative light and electron microscopic study of microsporogenesis in male-fertile and cytoplasmic male-sterile Sunflower (Helianthus annuus). In: Amer. J. Bot., 1977, vol. 64(6), 745-759. https://doi.org/10.1002/j.1537-2197.1977.tb11916.x
31. Smart, C., Moneger F., Leaver C.J. Cell-specific regulation of gene expression in mitochondria during another development in sunflower. In: The Plant Cell, 1994, vol. 6, 811-825. https://doi.org/10.1105/tpc.6.6.811
32. Vrânceanu, A.V. Aspecte noi privind cultura florii-soarelui. Editura Agro-Silvică: București 1967a, 30-45.
33. Zetsche, K., Horn, R. Molecular analysis of cytoplasmic male sterility in sunflower (Helianthus annuus L.). Plant Mitochondria. 1993, vol. 42, 411-422.
34. Makarenko, M., Kornienko, I., Azarin K., et al. Mitochondrial genomes organization in alloplasmic lines of sunflower (Helianthus annuus) with various types of cytoplasmic male sterility. In: PeerJ., 2018, nr. 6(e5266). https://doi.org/10.7717/peerj.5266
35. Horn, R., Hustedt, J.E., Horstmeyer, A., et al. The CMS-associated 16 kDa protein encoded by orfH522 in the PET1 cytoplasm is also present in other male-sterile cytoplasms of sunflower. In: Plant Molecular Biology, 1996, nr. 30(3), 523-538. https://doi.org/10.1007/BF00049329
36. Laveau, J.H., Schneider C., Berville, A. Microsporogenesis abortion in cytoplasmic male sterile plants from H. petiolaris or H. petiolaris fallax crossed by sunflower (Helianthus annuus). In: Ann. Bot., 1989, vol. 64 (2)137-148. https://doi.org/10.1093/oxfordjournals.aob.a087817
37. Balk, J., Leaver, C.J. The PET1 CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. In: The Plant Cell, 2001, vol. 13, 1803-1818. https://doi.org/10.1105/TPC.010116
38. Nizampatnam, N.R., Doodhi, H., Narasimhan, Y.K. et al. Expression of sunflower cytoplasmic male sterility-associated open reading frame, orfH522 induces male sterility in transgenic tobacco plants. In: Planta, 2009, nr. 229, 987-1001. https://doi.org/10.1007/s00425-009-0888-4
39. Nizampatnam, N.R., Kumar, V.D. Intron hairpin and transitive RNAi mediated silencing of orfH522 transcripts restores male fertility in transgenic male sterile tobacco plants expressing orfH522. In: Plant Molecular Biology, 2011, nr. 76, 557-573. https://doi.org/10.1007/s11103-011-9789-6
40. Touzet, P., Meyer, E. Cytoplasmic male sterility and mitochondrial metabolism in plants. In: Mitochondrion, 2014, nr. 19, 166-171. https://doi.org/10.1016/j.mito.2014.04.009
41. Goryunov, D.V., Anisimova, I.N. Gavrilova V.A., et al. Association mapping of fertility restorer gene for CMS PET1 in sunflower. In: Agronomy, 2019, vol. 9(49), 1-11. https://doi.org/10.3390/agronomy9020049
42. Polivanova, O.B., Sivolapova, A.B., Goryunov, D.V. et al. Structural diversity of sunflower (Helianthus annuus L.) candidate Rf1 loci based on gene-specific PCR. In: Research on Crops, 2021, vol. 22(1), 40-46. https://doi.org/10.31830/2348-7542.2021.034
43. Moneger, F., Smart, C., Leaver, C. Nuclear restoration of citoplasmic male sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. In: The EMBO Journal, 1994, nr. 13(1), 8-17. https://doi.org/10.1002/j.1460-2075.1994.tb06230.x
44. Duca, M., Port, A., Orozco-Cardenas, M., Lovat, C. Gibberellin-induced gene expression associated with cytoplasmic male sterility in Sunflower. In: Biotechnology & biotechnological equipment, 2008, nr. 22(2), 691-698. https://doi.org/10.1080/13102818.2008.10817536
45. Chhun T., Aya K., Asano K. et al. Gibberellin regulates pollen viability and pollen tube growth in rice. In: The Plant Cell, 2007, vol. 19, 3876-3888. https://doi.org/10.1105/tpc.107.054759
46. Griffiths J., Murase K., Rieu I. et al. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. In: The Plant Cell, 2006, 18, 33993414. https://doi.org/10.1105/tpc.106.047415
47. Duca, M., Port, A., Orozco-Cardenas, M. L., Lovatt, C. Mecanisme moleculare ale androsterilităţii ereditare şi induse la floarea-soarelui. În: Buletinul Academiei de Ştiințe a Moldovei. Ştiinţele Vieţii, 2006, nr. 1, 86-93.
48. Duca, M., Port, A., Orozco-Cardenas, M., Lovatt, C. Transcript analyses for mitochondrial sterile type rearrangement in sunflower. In: Romanian Biotechnological Letters, 2008, vol. 13(3), 3701-3706.
49. Arrieta-Montiel, M.P., Shedge, V., Davila, J. et al. Diversity of the Arabidopsis mitochondrial genome occurs via nuclear controlled recombination activity. In: Genetics, 2009, vol. 183(4), 1261-1268. https://doi.org/10.1534/genetics.109.108514
50. Gagliardi, D., Binder, S. Expression of the plant mitochondrial genome. In: Plant mitochondria (editor Logan D.C.): Blackwell Publishing, 2007, 50-96. https://doi.org/10.1002/9780470986592.ch3
51. Kmiec, B., Woloszynska, M., Janska, H. Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. In: Current Genetics, 2006, vol. 50, 149-159. https://doi.org/10.1007/s00294-006-0082-1
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