Abstract
Hybridizations involving different species are often hindered because of incompatibility reactions. Although these reproductive barriers have been observed in many plant species, the underlying mechanisms remain to be comprehensively elucidated. In this study, we detected a hybridization barrier between apple (Malus × domestica) and pear (Pyrus spp.) belonging to different genera in the subtribe Malinae of the family Rosaceae. Pollination experiments revealed that Pyrus pyrifolia (Japanese pear) pollen is compatible with Malus pistils, whereas Pyrus communis (European pear) pollen is not. These results imply there is a distinct cross-(in)compatibility reaction occurring in Pyrus species. Based on the varying pollen tube behaviors among Pyrus species, genetic analysis was conducted to identify the genomic region responsible for the intergeneric barrier. Malus–Pyrus intergeneric hybrids were used to detect distorted segregation regions by combining genome sequencing and fine-scale genotyping data. We defined a single locus on chromosome 5, in which P. pyrifolia-derived alleles were exclusively inherited to the intergeneric hybrids from the Pyrus interspecific hybrid. Of the 235 genes in this genomic region, 80 exhibited a specific pollen-expression pattern, including genes involved in self-incompatibility reactions. These candidate genes are herein discussed regarding their possible functions related to reproductive isolation.
Similar content being viewed by others
Data archiving statement
The datasets generated during the current study are available in the DDBJ SRA (Sequence Read Archive), under the BioProject number PRJDB8418.
References
Aguiar B, Vieira J, Cunha AE, Fonseca NA, Iezzoni A, Van Nocker S, Vieira CP (2015) Convergent evolution at the gametophytic self-incompatibility system in Malus and Prunus. PLoS One 10:e0126138
Akagi T, Henry IM, Tao R, Comai L (2014) A Y-chromosome–encoded small RNA acts as a sex determinant in persimmons. Science 346:646–650
Banno K, Hirano Y, Ishikawa H, Kakegawa M (2003) Breeding and characteristics of symmetric intergeneric hybrids between apple and pear. Acta Hortic 622:265–276
Bedinger PA, Chetelat RT, McClure B, Moyle LC, Rose JK, Stack SM, van der Knaap E, Baek YS, Lopez-Casado G, Covey PA, Kumar A, Li W, Nunez R, Cruz-Garcia F, Royer S (2011) Interspecific reproductive barriers in the tomato clade: opportunities to decipher mechanisms of reproductive isolation. Sex Plant Reprod 24:171–187
Bokszczanin K, Palucha A, Przybyla AA (2009) Description of a new trans-generic Skb-RNase allele in apple. Euphytica 166:83–94
Chetelat RT (2016) Overcoming sterility and unilateral incompatibility of Solanum lycopersicum × S. sitiens hybrids. Euphytica 207:319–330
Cheung AY, Wu HM (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Ann Rev Plant Biol 59:547–572
Daccord N, Celton JM, Linsmith G et al (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nature Genet 49:1099
De Franceschi P, Pierantoni L, Dondini L, Grandi M, Sansavini S, Sanzol J (2011) Evaluation of candidate F-box genes for the pollen S of gametophytic self-incompatibility in the Pyrinae (Rosaceae) on the basis of their phylogenomic context. Tree Genet Genomes 7:663–683
Fischer TC, Malnoy M, Hofmann T et al (2014) F1 hybrid of cultivated apple (Malus× domestica) and European pear (Pyrus communis) with fertile F2 offspring. Mol Breed 34:817–828
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224
Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156:1–13
Heng W, Wu J, Wu H, Cao Y, Nishio T, Zhang SL (2011) Recognition specificity of self-incompatibility in Pyrus and Malus. Mol Breed 28:549–557
Hua Z, Kao TH (2006) Identification and characterization of components of a putative Petunia S-locus F-box-containing E3 ligase complex involved in S-RNase-based self-incompatibility. Plant Cell 18:2531–2553
Inoue E, Sakuma F, Kasumi M, Hara H, Tsukihashi T (2003) Effect of high-temperature on suppression of the lethality exhibited in the intergeneric hybrid between Japanese pear (Pyrus pyrifolia Nakai) and apple (Malus× domestica Borkh.). Scientia Hortic 98:385–396
Kanaoka MM, Kawano N, Matsubara Y, Susaki D, Okuda S, Sasaki N, Higashiyama T (2011) Identification and characterization of TcCRP1, a pollen tube attractant from Torenia concolor. Ann Bot 108:739–747
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Kimura T, Sawamura Y, Kotobuki K, Matsuta N, Hayashi T, Ban Y, Yamamoto T (2003) Parentage analysis in pear cultivars characterized by SSR markers. J Japan Soc Hortic Sci 72:182–189
Lewis D, Crowe LK (1958) Unilateral interspecific incompatibility in flowering plants. Heredity 12:233–256
Li W, Chetelat RT (2010) A pollen factor linking inter- and intraspecific pollen rejection in tomato. Science 330:1827
Li W, Chetelat RT (2014) The role of a pollen-expressed Cullin1 protein in gametophytic self-incompatibility in Solanum. Genetics 196:439–442
Li W, Chetelat RT (2015) Unilateral incompatibility gene ui1. 1 encodes an S-locus F-box protein expressed in pollen of Solanum species. Proc Natl Acad Sci 112:4417–4422
Linsmith G, Rombauts S, Montanari S et al (2019) Pseudo-chromosome length genome assembly of a double haploid ‘Bartlett’ pear (Pyrus communis L.). doi. https://doi.org/10.1101/651778
Matsumoto D, Tao R (2016) Distinct self-recognition in the Prunus S-RNase-based gametophytic self-incompatibility system. Hortic J 85:289–305
Meng D, Gu Z, Yuan H, et al (2014) The microtubule cytoskeleton and pollen tube golgi vesicle system are required for in vitro S-RNase internalization and gametic self-incompatibility in apple. Plant and Cell Physiol 55, 977-989
Montanari S, Brewer L, Lamberts R et al (2016) Genome mapping of postzygotic hybrid necrosis in an interspecific pear population. Hortic Res 3:15064
Morimoto T, Banno K (2015) Genetic and physical mapping of Co, a gene controlling the columnar trait of apple. Tree Genet Genomes 11:807
Morimoto T, Kitamura Y, Numaguchi K, Akagi T, Tao R (2019) Characterization of post-mating interspecific cross-compatibility in Prunus (Rosaceae). Sci Hortic 246:693–699
Moyle LC, Jewell CP, Kostyun JL (2014) Fertile approaches to dissecting mechanisms of premating and postmating prezygotic reproductive isolation. Curr Opin Plant Biol 18:16–23
Ono K, Akagi T, Morimoto T, Wünsch A, Tao R (2018) Genome re-sequencing of diverse sweet cherry (Prunus avium) individuals reveals a modifier gene mutation conferring pollen-part self-compatibility. Plant Cell Physiol 59:1265–1275
Potter D, Eriksson T, Evans RC et al (2007) Phylogeny and classification of Rosaceae. Plant System Evol 266:5–43
Qin X, Li W, Liu Y, Tan M, Ganal M, Chetelat RT (2018) A farnesyl pyrophosphate synthase gene expressed in pollen functions in S-RNase-independent unilateral incompatibility. Plant J 93:417–430
Shimura I, Seike K, Shishikura T (1980) Intergeneic htbridization between Japanese pear, pyrus serotina Rehd. Var. culta Rehd, and apple, Malus pumila Mill. var. domestica Schneid. Japan J Breed 30, 170-180. (Japanese script with English abstract)
Sievers F, Wilm A, Dineen D et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539
Takada Y, Murase K, Shimosato-Asano H et al (2017) Duplicated pollen–pistil recognition loci control intraspecific unilateral incompatibility in Brassica rapa. Nature Plants 3:17096
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tovar-Méndez A, Kumar A, Kondo K, Ashford A, Baek YS, Welch L, Bedinger PA, McClure BA (2014) Restoring pistil-side self-incompatibility factors recapitulates an interspecific reproductive barrier between tomato species. Plant J 77:727–736
Tovar-Méndez A, Lu L, McClure B (2017) HT proteins contribute to S-RNase-independent pollen rejection in Solanum. Plant J 89:718–729
Tsuruta M, Mukai Y (2015) Hybrid seedling inviability locus (HIs1) mapped on linkage group 4 of the Japanese flowering cherry, Cerasus× yedoensis ‘Somei-yoshino’. Tree Genet Genome 11:88
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35(suppl_2), W71-W74.
Ushijima K, Sassa H, Tao R, Yamane H, Dandekar AM, Gradziel TM, Hirano H (1998) Cloning and characterization of cDNAs encoding S-RNases from almond (Prunus dulcis): primary structural features and sequence diversity of the S-RNases in Rosaceae. Mol Gen Genet 260:261–268
Velasco R, Zharkikh A, Affourtit J, et al (2010) The genome of the domesticated apple (Malus× domestica Borkh.). Nature Genet 42, 833
Yaegaki H, Yamaguchi M, Haji T, Suesada Y, Miyake M, Kihara T, Suzuki K, Uchida M (2012) New Japanese apricot cultivar ‘Tsuyuakane’. Bull NARO Inst Fruit Tree Sci 13, 1-6 (Japanese script with English abstract)
Yamamoto T, Kimura T, Shoda M, Imai T, Saito T, Sawamura Y, Kotobuki K, Hayashi T, Matsuta N (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:9–18
Acknowledgments
We appreciate the valuable comments and suggestions provided by Dr. Fabrizio Costa regarding the manuscript. We also thank Ms. Rieko Ishida and Mr. Yutaro Osako for maintaining plants during experiments.
Funding
This work was supported by the Overseas Research Fellowship provided by the Japan Society for the Promotion of Science (JSPS) to T.M. (201860070 and 19K15834). This study received financial assistance from the authors Drs Ryutaro Tao and Takashi Akagi [JSPS Grants-in-Aids for Scientific Research (A) (No. 15H02431) to RT and for Challenging Exploratory Research (No. 17K19265) to TA].
Author information
Authors and Affiliations
Contributions
T.M. conceived and designed the study. T.M., M.I., and K.B. conducted the experiments. T.M. analyzed the data. T.M. and A.I. drafted the manuscript. All authors approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Communicated by M. Troggio
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 482 kb)
Rights and permissions
About this article
Cite this article
Morimoto, T., Inaoka, M., Banno, K. et al. Genetic mapping of a locus controlling the intergeneric hybridization barrier between apple and pear. Tree Genetics & Genomes 16, 5 (2020). https://doi.org/10.1007/s11295-019-1397-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-019-1397-7