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Low temperature treatments of rice (Oryza sativa L.) anthers changes polysaccharide and protein composition of the anther walls and increases pollen fertility and callus induction

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Abstract

To understand the relationship between pollen fertility and callus induction from anthers of rice (Oryza sativa L.) during low-temperature treatment (LTT), F1 progeny of the cross ‘Nanjing 46’ × ‘Zaxima’ was used as materials. The pollen fertility, callus induction from anther and the histochemical and ultrastructural study of developing anthers from the rice plants with LTT was investigated. With LTT for 1–6 days before anther inoculation with callus induction medium, pollen fertility was maintained at 4 %. A moderate duration of LTT for 1–5 days and addition of exogenous plant growth regulators, 2,4-D from 1–2 mg L−1, or 0.3 mg L−1 KT, enhanced callus induction from anthers. A moderate duration of LTT altered the insoluble polysaccharide content in the anther wall. Compared with the untreated control at 25 °C, the insoluble polysaccharide content dramatically decreased in the anther wall within the first 2 days of LTT, and thereafter increased and peaked on the fifth day of LTT. On the fifth day of LTT, the protein content in the anther wall declined. No change in lipid content was observed during LTT. Electron microscopy showed that for the first 5 days of LTT, the integrity of the four-layer anther wall structure was maintained, and large numbers of cell organelles such as Golgi apparatus, endoplasmic reticulum and mitochondria were observed in the developing pollen grains. Plentiful amount of amyloplasts were also observed on the fourth day of LTT. At 7 days of LTT, the anther wall had been degraded to a single epidermal layer and the internal layers had disappeared. Thus, LTT for up to 5 days before anther inoculation in the IM medium may delay degradation of the innermost layer of the anther wall, the tapetum by altering the insoluble polysaccharide and protein contents in the anther wall.

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Abbreviations

2,4-D:

2,4-Dichlorophenoxyacetic acid

FAA:

Alcohol: formaldehyde: acetic acid

IAA:

Indole-3-acetic acid

iP:

Isopentenyladenine

KT:

Kinetin

LTT:

Low-temperature treatment

NAA:

1-Naphthaleneacetic acid

PAS:

Periodic acid-Schiff

References

  • Aarts MGM, Fiers MWEJ (2003) What drives plant stress genes? Trends Plant Sci 8:99–102. doi:10.1016/S1360-1385(03)00006-2

    Article  CAS  PubMed  Google Scholar 

  • Bishnoi U, Jain RK, Rohilla JS, Chowdhury VK, Gupta KR, Chowdhury JB (2000) Anther culture of recalcitrant indica × Basmati rice hybrids. Euphytica 114:93–101. doi:10.1023/A:1003915331143

    Article  CAS  Google Scholar 

  • Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. Plant Sci 174(3):483–494. doi:10.1111/j.1469-8137.2007.02060.x

    CAS  Google Scholar 

  • Castro JA, Clément C (2007) Sucrose and starch catabolism in the anther of Lilium during its development: a comparative study among the anther wall, locular fluid and microspore/pollen fractions. Planta 225:1573–1582. doi:10.1007/s00425-006-0443-5

    Article  CAS  PubMed  Google Scholar 

  • Chaudhary RC, Virmani SS, Khush GS (1981) Patterns of pollen abortion in some cytoplasmic- genetic male sterile lines of rice (Oryza sativa L.). Current outlook on hybrid rice 18:140–142

    Google Scholar 

  • Chu CY, Sun CS, Chu CC, Wang CC, Pi FY, Yiu KC, Hsu C (1975) Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Sci Sin (Peking) 18:659–668

    Google Scholar 

  • Datta R, Chamusco KC, Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130:1645–1656. doi:10.1104/pp.006908

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 111:137–145. doi:10.1104/pp/111/1/137

    CAS  PubMed Central  PubMed  Google Scholar 

  • Elias JM (1969) Effects of temperature, poststaining rinses and ethanol-butanol dehydrating mixtures on methyl green-pyronin staining. Biotech Histochem 44(4):201–204. doi:10.3109/10520296909063351

    Article  CAS  Google Scholar 

  • Feder N, O’brien TP (1968) Plant microtechnique: some principles and new methods. J Am Bot 55:123–142

    Article  Google Scholar 

  • Feher A, Pasternak TP, Dudits D (2003) Transient of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74(3):201–228. doi:10.1023/A:033216561

    Article  CAS  Google Scholar 

  • Forster BP, Herberle-Bors E, Kasha KJ, Touraev A (2007) The resurgence of haploids in higher plants. Trends Plant Sci 12:368–375. doi:10.1016/j.tplants.2007.06.007

    Article  CAS  PubMed  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229. doi:10.1105/tpc.5.10.1217

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grewal RK, Lulsdorf M, Crosser J, Ochatt S, Vandenberg A, Warkentin TD (2009) Doubled-haploid production in chickpea (Cicer arietinum L.): role of stress treatments. Plant Cell Rep 28:1289–1299. doi:10.1007/s00299-010-0844-6

    Article  CAS  PubMed  Google Scholar 

  • Gu HH, Hagberg P, Zhou WJ (2004) Cold pretreatment enhances microspore embryogenesis in oilseed rape (Brassica napus L.). Plant Growth Regul 42:137–143. doi:10.1023/B:GROW.0000017488.29181.fa

    Article  CAS  Google Scholar 

  • Hadrami IEL, D’auzac J (1992) Effects of growth regulators on polyamine content and peroxidase activity in Hevea brasiliensis callus. Ann Bot-London 69(4):323–325

    Google Scholar 

  • Han QX, Kang GZ, Guo TC (2013) Proteomic analysis of spring freeze-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.) Plant Physiol Bioch 63: 236–244. doi: 10.1016/j.plaphy.2012.12.002

  • Huang JH, Lu RJ, Sun YF, Zhou R (2002) Effects of different treatments on content of endogenous amino acid and microstructure of barley anthers. Acta Agricult Shanghai 18(4):8–13 (in Chinese)

    Google Scholar 

  • Islam SM, Tuteja N (2012) Enhancement of androgenesis by abiotic stress and other pretreatments in major crop species. Plant Sci 182:134–144. doi:10.1016/j.plantsci.2011.10.001

    Article  CAS  PubMed  Google Scholar 

  • Jähne A, Lörz H (1995) Cereal microspore culture. Plant Sci 109(1):1–12. doi:10.1016/0168-9452(95)04149-O

    Article  Google Scholar 

  • Jenner CF (1982) Storage of starch. Plant carbohydrates I. intracellular carbohydrates. Encyclopedia of plant physiology 13A Springer: Berlin, 700–747

  • Kiyosue T, Satoh S, Kamada H, Harada H (1993) Somatic embryogenesis in higher plants. J Plant Res 3:75–82

    Google Scholar 

  • Krogaard H, Andersen AS (1983) Free amino acids of Nicotiana alata anthers during development in vivo. Plant Physiol 57:527–531. doi:10.1111/j.1399-3054.1983.tb02780.x

    Article  CAS  Google Scholar 

  • Lásztity D, Rácz I, Páldi E (1999) Effect of long periods of low temperature exposure on protein synthesis activity in wheat seedlings. Plant Sci 149(1):59–62. doi:10.1016/S0168-9452(99)00143-0

    Article  Google Scholar 

  • Leyser O (2002) Molecular genetics of auxin signaling. Annu Rev Plant Biol 53:377–398. doi:10.1146/annurev.arplant.53.100301.135227

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zhao YT, Yan LN, Zhao YT (2008) Comparison in tissue culture power between anther in indica rice Yangdao 6 and japonica rice Suhuxiangjing. Nanjing normal university (Natural Science Edition) 131(4):108–111 (in Chinese)

    Google Scholar 

  • Li X, Wang C, Ren CG, Cong W, Jin L, Guo SW (2010) Change of microstructure in transgenic rice of pepc gene from maize with high photo efficiency under the strong light with 1-butanol treatment. Boreal Occident Sin 30:1614–1621 (in Chinese)

    CAS  Google Scholar 

  • LoSchiavo F, Filippini F, Cozzani F, Vallone D, Terzi M (1991) Modulation of auxin-binding proteins in cell suspensions I. Differential responses of carrot embryo cultures. Plant Physiol 97:60–64. doi:10.1104/pp.97.1.60

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • MacDonald MV, Aslam FN (1986) The effect of gamma irradiation on buds of Brassica napus ssp. Oleifera prior to anther culture. Crucif. Newslett 11: 90

  • Maheshwari SC, Tyagi AK, Malhotra K, Sopory SK (1980) Induction of haploidy from pollen grains in angiosperms-the current status. Theor Appl Genet 58:193–206. doi:10.1007/BF00288437

    Article  CAS  PubMed  Google Scholar 

  • Martha CW, Sandra MR, Joyce AB, Wynne JC (1991) Effect of microspore stage and media on anther culture of peanut (Arachis hypogaea L.). Plant Cell, Tissue Organ Cult 24:25–28. doi:10.1007/BF00044261

    Article  Google Scholar 

  • Michalczuk L, Ribnicky DM, Cooke TJ, Cohen JD (1992) Regulation of indole-3- acetic acid biosynthetic pathways in carrot cell cultures. Plant Physiol 100(3):1346–1353. doi:10.1104/pp.100.3.1346

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Milloning G (1962) Further observations on a phosphate buffer for osmium solutions in fixation. In: Proceeding 5th Intern. Conf. Electron Microscopy, Philadelphia 1962, vol. II, ed. Breese, S. S. New York, Academic Press, p. 8

  • Muñoz-Amatriaín M, Svensson JT, Castillo AM, Cistué L, Close TJ. Vallés MP (2009) Expression profiles in barley microspore embryogenesis. Adv Haploid Product Higher Plants 127–134

  • Pacini E, Franchi GG, Hesse M (1985) The tapetum: its form, function, and possible phylogeny in Embryophyta. Plant Syst Evol 149(3–4):155–185. doi:10.1007/BF00983304

    Article  Google Scholar 

  • Pan ZY, Zhu SP, Guan R, Deng XX (2010) Identification of 2,4-D-responsive proteins in embryogenic callus of Valencia sweet orange (Citrus sinensis Osbeck) following osmotic stress. Plant Cell Tissue Organ Culture 103:145–153. doi:10.1007/s11240-010-9762-0

    Article  CAS  Google Scholar 

  • Pearse AGE (ed.) (1985) Histochemistry. Theoretical and Applied vol. 2: Analytical technology, (4th edn). Churchill Livingstone Inc., Edinburgh, UK

  • Peng M, Ziauddin A, Wolyn DJ (1997) Development of asparagus microspores in vivo and in vitro is influenced by gametogenic stage and cold treatment. In Vitro Cell Dev Biol Plant 33:263–268. doi:10.1007/s11627-997-0047-1

    Article  Google Scholar 

  • Ren CG, Li X, Liu XL, Wei XD, Dai CC (2014) Hydrogen peroxide regulated photosynthesis in C 4 -pepc transgenic rice. Plant Physiol Biochem 74:218–229. doi:10.1016/j.plaphy.2013.11.011

    Article  CAS  PubMed  Google Scholar 

  • Rey HY, Sansberro PA, Collavino MM, Davina JR, Gonzales AM, Mroginski LA (2002) Colchicine, trifluralin, and oryzalin promoted development of somatic embryos in Ilex paraguariensis (Aquifoliaceae). Euphytica 123:49–56. doi:10.1023/A:1014489207888

    Article  CAS  Google Scholar 

  • Sangwan RS, Sangwan-Norreel BS (1987) Biochemical cytology of pollen embryogenesis. Int Rev Cytol 107:221–272

    Article  Google Scholar 

  • Sasaki K, Shimomura K, Kamada H, Harada H (1994) IAA metabolism in embryogenic and non-embryogenic carrot cells. Plant Cell Physiol 35(8):1159–1164

    CAS  Google Scholar 

  • Shi SL, Ding D, Mei SY, Wang JB (2010) A comparative light and electron microscopic analysis of microspore and tapetum development in fertile and cytoplasmic male sterile radish. Protoplasma 241:37–49. doi:10.1007/s00709-009-0100-5

    Article  PubMed  Google Scholar 

  • Shim YS, Kasha KJ (2003) The influence of pretreatment on cell stage progression and the time of DNA synthesis in barley (Hordeum vulgare L.) uninucleate microspores. Plant Cell Rep 21:1065–1071. doi:10.1007/s00299-003-0635-4

    Article  CAS  PubMed  Google Scholar 

  • Shivanna KR, Cresti M, Ciampolini F, Sawhney VK (1997) Pollen development and pollen-pistil interaction. Pollen biotechnology for crop production and improvement. Cambridge University, Cambridge UK, pp 15–39

    Google Scholar 

  • Sunderland N, Huang B, Hills GJ (1984) Disposition of pollen in situ and its relevance to anther/pollen culture. J Exp Bot 35(4):521–530. doi:10.1093/jxb/35.4.521

    Article  Google Scholar 

  • Touraev A, Vicente O, Heberle-Bors E (1997) Initiation of microspore embryogenesis by stress. Trends Plant Sci 2:297–302. doi:10.1016/S1360-1385(97)89951-7

    Article  Google Scholar 

  • Tütüncü Konyar S, Dane F (2013) Cytochemistry of pollen development in Campsis radicans (L.) Seem. (Bignoniaceae). Plant Syst Evol 299:87–95. doi:10.1007/s00606-012-0705-6

    Article  Google Scholar 

  • Tütüncü Konyar S, Dane F, Tütüncu S (2013) Distribution of insoluble polysaccharides, neutral lipids, and proteins in the developing anthers of Campsis radicans (L.) Seem. (Bignoniaceae). Plant Syst Evol 299:743–760. doi:10.1007/s00606-013-0758-1

    Article  Google Scholar 

  • Vergne P, Riccardi F, Beckert M, Dumas C (1990) Detection of androgenesis related proteins in Maize. Progress in plant cellular and molecular biology, current plant science and biotechnology in agriculture 416–421

  • Willcox MC, Sandra Reed M, Burns JA, Wynne JC (1991) Effect of microspore stage and media on anther culture of peanut (Arachis hypogaea L.). Plant Cell, Tissue Organ Cult 24:25–28. doi:10.1007/BF00044261

    Article  Google Scholar 

  • Xie JH, Gao MW, Liang ZQ, Shu QY, Cheng XY, Xue QZ (1997) The effect of cool pretreatment on the isolated microspore culture and the free amino acid change of anthers in Japonica rice (Oryza sativa L.). J Plant Physiol 151:79–82. doi:10.1016/S0176-1617(97)80040-5

    Article  CAS  Google Scholar 

  • Zaki MAM, Dickinson HG (1991) Microspore-derived embryos in Brassica: the significance of division symmetry in pollen mitosis I to embryogenic development. Sexual Plant Rep 4:48–55. doi:10.1007/BF00194572

    Google Scholar 

  • Zhang L, Bai XJ (2011) Effect of pretreatments on physiological and biochemical characteristics in isolated anthers of radish (Raphanus sativus L.). Acta Agricult Boreali-Occidentalis Sinica 20(7): 60–63(in Chinese)

  • Zhang DB, Yang L (2014) Specification of tapetum and microsporocyte cells within the anther. Curr Opin Plant Biol 17:49–55

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman JL (1993) Somatic embryogenesis: a model for early development in higher plants. Plant Cell 5:1411–1423

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (Nos. 30871459 and 31371554), the Agricultural Science and Technology Innovation Fund of Jiangsu in China [(CX(14)5004)] and the Natural Science Foundation of Jiangsu Province (No. BK21378). The authors thank the anonymous reviewers and editorial staff for their time and attention.

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Correspondence to X. Li.

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Q. Q. Tian and C. M. Lu have contributed to this work equally.

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Tian, Q.Q., Lu, C.M., Li, X. et al. Low temperature treatments of rice (Oryza sativa L.) anthers changes polysaccharide and protein composition of the anther walls and increases pollen fertility and callus induction. Plant Cell Tiss Organ Cult 120, 89–98 (2015). https://doi.org/10.1007/s11240-014-0582-5

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