Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-28T13:20:39.612Z Has data issue: false hasContentIssue false
  • English
  • Français

Callose depositions underlie the incompatible reaction in intergeneric crosses of rice

Published online by Cambridge University Press:  13 October 2021

Karminderbir Kaur ,
Mehak Gupta ,
Yogesh Vikal Open the ORCID record for Yogesh Vikal [Opens in a new window] ,
Kuldeep Singh  and
Kumari Neelam Open the ORCID record for Kumari Neelam [Opens in a new window]
Karminderbir Kaur
Affiliation:
School of Agricultural Biotechnology, Punjab Agricultural University, Ludhiana 141004, India
Mehak Gupta
Affiliation:
Department of Plant Breeding and Genetics, Punjab Agricultural University, Ludhiana 141004, India
Yogesh Vikal
Affiliation:
School of Agricultural Biotechnology, Punjab Agricultural University, Ludhiana 141004, India
Kuldeep Singh
Affiliation:
School of Agricultural Biotechnology, Punjab Agricultural University, Ludhiana 141004, India National Bureau of Plant Genetic Resources, PUSA Campus, New Delhi 110012, India
Kumari Neelam*
Affiliation:
School of Agricultural Biotechnology, Punjab Agricultural University, Ludhiana 141004, India
*
Author for correspondence: Kumari Neelam, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Distant hybridization of cereals is often impaired by fertilization barriers. Haploid induction through intergeneric crossing is well developed in wheat but has not been successful in rice due to incompatibility issues. The present study was thus undertaken to identify fertilization barriers that hinder the compatibility of the rice cultivar Punjab Rice 121 with maize and pearl millet lines as pollinators. A total of 37,357 spikelets were pollinated, yielding 494 caryopses upon supplementation with auxins. The resultant caryopses, arising from true intergeneric crosses, lacked embryos. Imaging of the pollinated pistils at different intervals indicated that intense callose depositions block the release of generative nuclei to the ovule in these wide crosses. Rice spikelets pollinated with rice pollen (cis-generic crosses) exhibited positive indicators of fertilization reaction at the micropyle. While the cis-generic crosses initiated true caryopsis formation after 24 h, no comparative reaction was observed in the intergeneric crosses. The current survey underlines that the rice female gametophyte presents a strong pre-fertilization barrier to foreign pollen. This barrier may be modulated in the future by altering genotype and auxin combinations.

Keywords

Callose depositionfertilization barriersincompatibilityintergeneric hybridizationwide crosses of rice
Type
Research Article
Information
Plant Genetic Resources , Volume 19 , Issue 5 , October 2021 , pp. 447 - 452
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of NIAB

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, F and Comeau, A (1990) Wheat × pearl millet hybridization: consequence and potential. Euphytica 50, 181–190.CrossRefGoogle Scholar
Ballesfin, ML, Vinarao, RB, Sapin, J, Kim, SR and Jena, KK (2018) Development of an intergeneric hybrid between Oryza sativa L. and Leersia perrieri (A. Camus) Launert. Breeding Science 68, 474–480. doi: 10.1270/jsbbs.18045.CrossRefGoogle ScholarPubMed
Baum, M, Lagudah, ES and Appels, R (1992) Wide crosses in cereals. Annual Review Plant Physiology and Plant Molecular Biology 43, 117–143.CrossRefGoogle Scholar
Cresti, M and Van Went, JL (1976) Callose deposition and plug formation in Petunia pollen tubes in situ. Planta 133, 35–40.CrossRefGoogle ScholarPubMed
Deming, Z, Shanbao, C, Xiaolan, D, Junhua, F, Xianbin, S, Yonghui, L, Liancheng, L and Bensong, X (1985) Genetic variations in the hybrids of rice (Oryza sativa) and sorghum (Sorghum vulgare). Theoretical and Applied Genetics 70, 542–547.CrossRefGoogle Scholar
Dong, X, Hong, Z, Sivaramakrishnan, M, Mahfouz, M and 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.CrossRefGoogle ScholarPubMed
Dumas, C and Knox, RB (1983) Callose and determination of pistil viability and incompatibility. Theoretical and Applied Genetics 67, 1–10.CrossRefGoogle ScholarPubMed
Gaget, M, Said, C, Dumas, C and Knox, RB (1984) Pollen-pistil interactions in interspecific crosses of Populus (sections Aigeiros and Leuce): pollen adhesion, hydration and callose responses. Journal of Cell Science 72, 173–184.CrossRefGoogle ScholarPubMed
García-Llamas, C, Ramirez, MC and Ballesteros, J (2004) Effect of pollinator on haploid production in durum wheat crossed with maize and pearl millet. Plant Breeding 123, 201–203.CrossRefGoogle Scholar
Gernand, D, Rutten, T, Varshney, A, Rubtsova, M, Prodanovic, S, Brüß, C, Kumlehn, J, Matzk, F and Houben, A (2005) Uniparental chromosome elimination at mitosis and interphase in wheat and pearl millet crosses involves micronucleus formation, progressive heterochromatinization, and DNA fragmentation. The Plant Cell 17, 2431–2438.CrossRefGoogle ScholarPubMed
Heslop-Harrison, J (1975) Incompatibility and the pollen-stigma interaction. Annual Review of Plant Physiology 26, 403–425.CrossRefGoogle Scholar
Heslop-Harrison, J (1982) Pollen-stigma interaction and cross-incompatibility in the grasses. Science 215, 1358–1364.CrossRefGoogle ScholarPubMed
Inagaki, MN (1997) Technical advances in wheat haploid production using ultra-wide crosses. JIRCAS J 4, 51–62.Google Scholar
Inagaki, MN and Hash, CT (1998) Production of haploids in bread wheat, durum wheat and hexaploid triticale crossed with pearl millet. Plant Breeding 117, 485–487.CrossRefGoogle Scholar
Inagaki, M and Mujeeb-Kazi, A (1995) Comparison of polyhaploid production frequencies in crosses of hexaploid wheat with maize, pearl millet and sorghum. Japanese Journal of Breeding 45, 157–161.CrossRefGoogle Scholar
Jamwal, NS, Chaudhary, HK, Badiyal, A and Hussain, W (2016) Factors influencing crossability among triticale and wheat and its subsequent effect along with hybrid necrosis on haploid induction. Acta Agriculturae Scandinavia. Section B-Soil and Plant Science 66, 282–289.Google Scholar
Jelodar, NB, Blackhall, NW, Hartman, TPV, Brar, DS, Khush, G, Davey, MR, Cocking, EC and Power, JB (1999) Intergeneric somatic hybrids of rice [Oryza sativa L.(X) Porteresia coarctata (Roxb.) Tateoka]. Theoretical and Applied Genetics 99, 570–577.CrossRefGoogle Scholar
Jena, KK (1994) Production of intergeneric hybrid between Oryza sativa L. and Porteresia coarctata T. Current Science 67, 744–746.Google Scholar
Kapoor, R and Singh, G (2017) An attempt to produce oat haploids using oat × maize hybridization. International Journal of Pure Applied Bioscience 5, 234–240.CrossRefGoogle Scholar
Kaushal, P and Sidhu, JS (2000) Pre-fertilization incompatibility barriers to interspecific hybridizations in Pennisetum species. Journal of Agricultural Science 134, 199–206.CrossRefGoogle Scholar
Laurie, DA and Bennett, MD (1986) Wheat × maize hybridization. Canadian Journal of Genetics and Cytology 28, 313–316.CrossRefGoogle Scholar
Laurie, DA and Snape, JW (1990) The agronomic performance of wheat doubled haploid lines derived from wheat × maize crosses. Theoretical and Applied Genetics 79, 813–816.CrossRefGoogle ScholarPubMed
Luna, E, Pastor, V, Robert, J, Flors, V, Mauch-Mani, B and Ton, J (2011) Callose deposition: a multifaceted plant defense response. Molecular Plant Microbe Interaction 24, 183–193.CrossRefGoogle ScholarPubMed
Mahato, A and Chaudhary, HK (2019) Auxin induced haploid induction in wide crosses of Durum wheat. Cereal Research Communications 47, 552–565.10.1556/0806.47.2019.31CrossRefGoogle Scholar
Mujeeb-Kazi, A and Riera-Lizarazu, O (1997) Polyhaploid production in the triticeae by sexual hybridization. In Mohan Jain, S, Spory, SK and Veilleux, RE (eds), In Vitro Haploid Production in Higher Plants. Dordrecht: Kluwer, pp. 276–295.Google Scholar
Murashige, T and Skoog, F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.CrossRefGoogle Scholar
Nezu, M, Katayama, TC and Kihara, H (1960) Genetic study of the genus Oryza. I. Crossability and chromosomal affinity among 17 species. Seiken ZihO 11, 1–11.Google Scholar
Niroula, RK and Bimb, HP (2009) Overview of wheat × maize system of crosses for dihaploid induction in wheat. World Applied Sciences Journal 7, 1037–1045.Google Scholar
Sarker, RH, Samad, MA, Seraj, ZI, Hoque, MI and Islam, AS (1993) Pollen tube growth in crosses between Porteresia coarctata and Oryza sativa. Euphytica 69, 129–134.CrossRefGoogle Scholar
Sedgley, M (1977) Reduced pollen tube growth and the presence of callose in the pistil of the male floral stage of the avocado. Scientia Horticulturae 7, 27–36.CrossRefGoogle Scholar
Shivanna, KR, Heslop-Harrison, Y and Heslop-Harrison, J (1978) The pollen-stigma interaction: bud pollination in the Cruciferae. Acta Botanica Neerlandica 27, 107–119.CrossRefGoogle Scholar
Sitch, LA (1990) Incompatibility barriers operating in crosses of Oryza sativa with related species and genera. In Gustafson JP (ed) Gene Manipulation in Plant Improvement II. Boston, MA: Plenum Press, pp. 77–93.CrossRefGoogle Scholar
Sitch, LA and Romero, GO (1990) Attempts to overcome prefertilization incompatibility in interspecific and intergeneric crosses involving Oryza sativa L. Genome 33, 321–327.CrossRefGoogle Scholar
Sitch, LA, Romero, GO and Dalmacior, D (1989) Preliminary studies on pollen grain germination and pollen tube growth in crosses of Oryza sativa and Porteresia coarctata. International Rice Research Newsletter 14, 5.Google Scholar
Srivastava, P and Bains, NS (2018) Accelerated wheat breeding: doubled haploids and rapid generation advance. In Gosal SS and Wani SH (eds) Biotechnologies of Crop Improvement, vol. 1. Cham: Springer, pp. 437–461.CrossRefGoogle Scholar
Stebbins, GL (1958) The inviability, weakness and sterility of interspecific hybrids. Advances in Genetics 9, 147–215.CrossRefGoogle ScholarPubMed
Stott, KG (1972) Pollen germination and pollen-tube characteristics in a range of apple cultivars. Journal of Horticultural Science 47, 191–198.CrossRefGoogle Scholar
Suenaga, K (1994) Doubled haploid system using the intergeneric crosses between wheat (Triticum aestivum) and maize (Zea mays) (No. 95-050005. CIMMYT.).Google Scholar
Sulaman, W, Arnoldo, M, Yu, K, Tulsieram, L, Rothstein, SJ and Goring, DR (1997) Loss of callose in the stigma papillae does not affect the Brassica self-incompatibility phenotype. Planta 203, 327–331.CrossRefGoogle Scholar
Unal, M (1986) A comparative cytological study on compatible and incompatible pollen tubes of Petunia hybrida. Istanbul Universitesi Fen Fakultesi mecmuasi Seri 51, 1–12.Google Scholar
Wedzony, and van Lammeren, (1996) Pollen tube growth and early embryogenesis in wheat x maize crosses influenced by 2-4-D. Annals of Botany 77, 639–648.CrossRefGoogle Scholar
Zenkteler, M and Nitzsche, W (1984) Wide hybridization experiments in cereals. Theoretical and Applied Genetics 68, 311–315.CrossRefGoogle ScholarPubMed