Protoplasma

, Volume 255, Issue 3, pp 751–759 | Cite as

ABA and IAA control microsporogenesis in Petunia hybrida L.

  • L. V. Kovaleva
  • A. S. Voronkov
  • E. V. Zakharova
  • I. M. Andreev
Original Article

Abstract

The formation of fertile male gametophyte is known to require timely degeneration of polyfunctional tapetum tissue. The last process caused by the programmed cell death (PCD) is a part of the anther program maturation which leads to sequential anther tissue destruction coordinated with pollen differentiation. In the present work, distribution of abscisic acid (ABA) and indole-3-acetic acid (IAA) in developing anthers of male-fertile and male-sterile lines of petunia (Petunia hybrida L.) was analyzed by using the immunohistochemical method. It was established that the development of fertile male gametophyte was accompanied by monotonous elevation of ABA and IAA levels in reproductive cells and, in contrast, their monotonous lowering in tapetum cells and the middle layers. Abortion of microsporocytes in the meiosis prophase in the sterile line caused by premature tapetum degeneration along with complete maintenance of the middle layers was accompanied by dramatic, twofold elevation in the levels of both the phytohormones in reproductive cells. The data obtained allowed us to conclude that at the meiosis stage ABA and IAA are involved in the PCD of microsporocytes.

Keywords

Petunia hybrida Male sterility Tapetum PCD ABA IAA 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Albacete A, Cantero-Navarro E, Großkinsky DK, Arias CL, Balibrea ME, Bru R, Fragner L, Ghanem ME, de la González M, Hernández JA et al (2015) Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato. J Exp Bot 66(3):863–878.  https://doi.org/10.1093/jxb/eru448 CrossRefPubMedGoogle Scholar
  2. Aloni R, Aloni E, Langhans V, Ullrich CI (2006) Role of auxin in regulating arabidopsis flower development. Planta 223(2):315–328.  https://doi.org/10.1007/s00425-005-0088-9 CrossRefPubMedGoogle Scholar
  3. Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, León P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 14(16):2085–2096PubMedPubMedCentralGoogle Scholar
  4. Benschop JJ, Jackson MB, Gahl K, Vreeburg RA, Croker SJ, Peeters AJ, Voesenck LA (2005) Contrasting interactions between ethylene and abscisic acid in Rumex species differing in submergence tolerance. Plant J 44(5):756–768.  https://doi.org/10.1111/j.1365-313X.2005.02563.x CrossRefPubMedGoogle Scholar
  5. Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20(7):1760–1774.  https://doi.org/10.1105/tpc.107.057570 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cecchetti V, Celebrin D, Napoli N, Ghelli R, Brunetti P, Costantino P, Cardarelli M (2016) An auxin maximum in the middle layer controls stamen development and pollen maturation in Arabidopsis. New Phytol 213(3):1194–1207.  https://doi.org/10.1111/nph.14207 CrossRefPubMedGoogle Scholar
  7. Chen D, Zhao J (2008) Free IAA in stigmas and styles during pollen germination and pollen tube growth of Nicotiana tabacum. Physiol Plant 134(1):202–215.  https://doi.org/10.1111/j.1399-3054.2008.01125.x CrossRefPubMedGoogle Scholar
  8. Chen D, Ren Y, Deng Y, Zhao J (2010) Auxin polar transport is essential for the development of zygote and embryo in Nicotiana tabacum L. and correlated with ABP1 and PM H+-ATPase activities. J Exp Botany 61:1853–1867CrossRefGoogle Scholar
  9. Dal Bosco C, Dovzhenko A, Palme K (2012) Intracellular auxin transport in pollen: PIN8, PIN5 and PILS5. Plant Signal Behav 7(11):1504–1505.  https://doi.org/10.4161/psb.21953 CrossRefPubMedPubMedCentralGoogle Scholar
  10. De Storme N, Geelen D (2014) The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant Cell Environ 37(1):1–18.  https://doi.org/10.1111/pce.12142 CrossRefPubMedGoogle Scholar
  11. Dobrovol’skaya AA, Rodionova GB, Voronkov AS, Kovaleva LV (2009) Sporophyte-gametophyte interactions between anther and male gametophyte in petunia. Rus J Plant Physiology 56(3):394–401.  https://doi.org/10.1134/S1021443709030133 CrossRefGoogle Scholar
  12. Dong Z, Yu Y, Li S, Wang J, Tang S, Huang R (2016) Abscisic acid antagonizes ethylene production through the ABI4-mediated transcriptional repression of ACS4 and ACS8 in Arabidopsis. Mol Plant 9(1):126–135.  https://doi.org/10.1016/j.molp.2015.09.007 CrossRefPubMedGoogle Scholar
  13. Dorion S, Lalonde S, Saini HS (1996) Induction of male sterility in wheat by meiotic-stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiol 111(1):137–145.  https://doi.org/10.1104/pp.111.1.137 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Eckardt NA (2002) Abscisic acid biosynthesis gene underscores the complexity of sugar, stress, and hormone interactions. Plant Cell 14(11):2645–2649.  https://doi.org/10.1105/tpc.141110 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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. Ann Bot 112(6):1045–1055.  https://doi.org/10.1093/aob/mct173 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Feng XL, Ni WM, Elge S, Mueller-Roeber B, Xu ZH, Xue HW (2006) Auxin flow in anther filaments is critical for pollen grain development through regulating pollen mitosis. Plant Mol Biol 61(1-2):215–226.  https://doi.org/10.1007/s11103-006-0005-z CrossRefPubMedGoogle Scholar
  17. Friml J (2010) Subcellular trafficking of PIN auxin efflux carriers in auxin transport. Eur J Cell Biol 89(2-3):231–235.  https://doi.org/10.1016/j.ejcb.2009.11.003 CrossRefPubMedGoogle Scholar
  18. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124(4):509–525.  https://doi.org/10.1007/s10265-011-0412-3 CrossRefPubMedGoogle Scholar
  19. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5(10):1217–1229.  https://doi.org/10.1105/tpc.5.10.1217 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gómez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 7:876–891CrossRefGoogle Scholar
  21. Hirano K, Aya K, Hobo T, Sakakibara H, Kojima M, Shim RA, Hasegawa Y, Ueguch-Tanaka M, Matsuoka M (2008) Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol 49(10):1429–1450.  https://doi.org/10.1093/pcp/pcn123 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Ishimaru K, Takada K, Watanabe S, Kamada H, Ezura H (2006) Stable male sterility induced by the expression of mutated melon ethylene receptor genes in Nicotiana tabacum. Plant Sci 171(3):355–359.  https://doi.org/10.1016/j.plantsci.2006.04.006 CrossRefPubMedGoogle Scholar
  23. Ji X, Dong B, Shiran B, Talbot MJ, Edlington JE, Hughes T, White RG, Gubler F, Dolferus R (2011) Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiol 156(2):647–662.  https://doi.org/10.1104/pp.111.176164 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kovaleva LV, Dobrovolskaya A, Voronkov A, Rakitin V (2011) Ethylene is involved in the control of male gametophyte development and germination in petunia. J Plant Growth Regul 30(1):64–73.  https://doi.org/10.1007/s00344-010-9168-6 CrossRefGoogle Scholar
  25. Kovaleva L, Voronkov A, Zakharova E, Minkina Y, Timofeeva G, Andreev I (2016) Regulation of petunia pollen tube growth by phytohormones: identification of their potential targets. J Agric Sci Technol A 6:239–254.  10.17265/2161–6256/2016.04.004 Google Scholar
  26. Kovaleva LV, Zakharova EV, Voronkov AS, Timofeeva GV (2017a) Auxin abolishes inhibitory effects of methylcyclopropen and amino oxyacetic acid on pollen grain germination, pollen tube growth, and the synthesis of ACC in petunia. Russ J Dev Biol 48(2):122–129.  https://doi.org/10.1134/S1062360417020059 CrossRefGoogle Scholar
  27. Kovaleva LV, Zakharova EV, Voronkov AS, Timofeeva GV, Andreev IM (2017b) Role of abscisic acid and ethylene in the control of water transport-driving forces in germinating petunia male gametophyte. Russ J Plant Physiol 64(5):782–793.  https://doi.org/10.1134/S1021443717040070 CrossRefGoogle Scholar
  28. Ku S, Yoon H, Suh HS, Chung YY (2003) Male-sterility of thermosensitive genic male- sterile rice is associated with premature programmed cell death of the tapetum. Planta 217(4):559–565.  https://doi.org/10.1007/s00425-003-1030-7 CrossRefPubMedGoogle Scholar
  29. León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8(3):110–116.  https://doi.org/10.1016/S1360-1385(03)00011-6 CrossRefPubMedGoogle Scholar
  30. Mileykovskaya E, Dowhan W (2000) Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange. J Bacteriol 182(4):1172–1175.  https://doi.org/10.1128/JB.182.4.1172-1175.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Oliver SN, Dennis ES, Dolferus R (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol 48(9):1319–1330.  https://doi.org/10.1093/pcp/pcm100 CrossRefPubMedGoogle Scholar
  32. Phan HA, Iacuone S, Li SF, Parish RW (2011) The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana. Plant Cell 23(6):2209–2224.  https://doi.org/10.1105/tpc.110.082651 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9(12):606–613.  https://doi.org/10.1016/j.tplants.2004.10.009 CrossRefPubMedGoogle Scholar
  34. Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugur input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3(6):942–955.  https://doi.org/10.1093/mp/ssq044 CrossRefPubMedGoogle Scholar
  35. Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, Higashitani N, Miyazawa Y, Takahashi H, Watanabe M, Higashitani A (2010) Auxins reverse plant male sterility caused by high temperatures. Proc Natl Acad Sci U S A 107(19):8569–8574.  https://doi.org/10.1073/pnas.1000869107 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Sharma KD, Nayar H (2016) Regulatory networks in pollen development under cold stress. Front Plant Sci 7:402.  https://doi.org/10.3389/fpls.2016.00402 PubMedPubMedCentralGoogle Scholar
  37. Sundberg E, Østergaard L (2009) Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb Perspect Biol 1(6):a001628.  https://doi.org/10.1101/cshperspect.a001628 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Vizcay-Barrena G, Wilson ZA (2006) Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. J Exp Bot 57(11):2709–2717.  https://doi.org/10.1093/jxb/erl032 CrossRefPubMedGoogle Scholar
  39. Wang M, Hoekstra S, van Bergen S, Lamers GE, Oppedijk BJ, van der Heijden MW, de Priester Schilperoort RA (1999) Apoptosis in developing anthers and the role of ABA in this process during androgenesis in Hordeum vulgare L. Plant Mol Biol 39(3):489–501.  https://doi.org/10.1023/A:1006198431596 CrossRefPubMedGoogle Scholar
  40. Wilson ZA, Song J, Taylor B, Yang C (2011) The final split: the regulation of anther dehiscence. J Exp Bot 62(5):1633–1649.  https://doi.org/10.1093/jxb/err014 CrossRefPubMedGoogle Scholar
  41. Zazímalová E, Murphy AS, Yang H, Hoyerová K, Hosek P (2010) Auxin transporters—why so many? Cold Spring Harb Perspect Biol 2:a001552CrossRefPubMedPubMedCentralGoogle Scholar
  42. Zhang D, Yang L (2014) Specification of tapetum and microsporocyte cells within the anther. Curr Opin Plant Biol 17:49–55.  https://doi.org/10.1016/j.pbi.2013.11.001 CrossRefPubMedGoogle Scholar
  43. Zhu Y, Dun X, Zhou Z, Xia S, Yi B, Wen J, Shen J, Ma C, Tu J, Fu T (2010) A separation defect of tapetum cells and microspore mother cells results in male sterility in Brassica napus: the role of abscisic acid in early anther development. Plant Mol Biol 72(1-2):111–123.  https://doi.org/10.1007/s11103-009-9556-0 CrossRefPubMedGoogle Scholar
  44. Żur I, Dubas E, Krzewska M, Waligórski P, Dziurka M, Janowiak F (2015) Hormonal requirements for effective induction of microspore embryogenesis in triticale (× Triticosecale Wittm.) anther cultures. Plant Cell Rep 34(1):47–62.  https://doi.org/10.1007/s00299-014-1686-4 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  2. 2.State Humanitarian-Technological UniversityOrekhovo-ZuyevoRussia
  3. 3.Russian State Agrarian University–Agricultural Academy named by TimiryazevMoscowRussia

Personalised recommendations