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Inheritance of the lethal alleles in the Pyrus PEAR3 × ‘Moonglow’ pedigree. Progenitors of PEAR3 and ‘Moonglow’ were scanned with SSR markers mapped within the regions involved in HN. For each marker, the incompatible allele (in bp) is highlighted in red.
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Deleterious epistatic interactions in plant inter- and intraspecific hybrids can cause a phenomenon known as hybrid necrosis, characterized by a typical seedling phenotype whose main distinguishing features are dwarfism, tissue necrosis and in some cases lethality. Identification of the chromosome regions associated with this type of incompatibilit...
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... Simple inheritance of NHR appears to be corroborated by the resistance to V. nashicola in European pears 'La France' and 'Bartlett' having been attributed to a single dominant, homozygous resistance locus, Vn (Abe et al. 2000). However, the data from the latter study could also be interpreted as the European pear cultivars each to carry a second gene for resistance (Supplementary Material 1), although segregation distortions may have played a role, too (Montanari et al. 2016). Both an unspecified QTL from 'La France' (Yamamoto et al. 2009), and the Rvn2 locus for resistance derived from 'Bartlett'/'Williams Bon Chretien' (Cho et al. 2009;Bouvier et al. 2012) were mapped to the same region of linkage group (LG) 2. They both are assumed to be NHR genes, or possibly even the same gene, for V. nashicola resistance in these European pears (Bouvier et al. (2012). ...
... More recently, the Rvn3 gene originating from 'Bartlett', too, was mapped to LG6 of 'Greensis' (Oh et al. 2021), supporting the twogene NHR hypothesis in at least 'Bartlett' . In contrast, necrotic reactions characterized by symptoms without sporulation on some Asian pears infected with V. nashicola were suggested to be controlled by quantitative trait loci (QTL) (Abe and Kotobuki 1998) in addition to the 'host' resistance gene Vnk gene on LG1 of 'Kinchaku' (Terakami et al. 2006), which later was re-named Rvn1 (Montanari et al. 2016); an unnamed gene in 'Huangguan' (Dong et al. 2010); and Rvn4 on LG7 of 'Hong Li' . ...
... The observed segregation distortion could be genetically explained. Montanari et al. (2016) observed similar segregation distortion. Despite a low incompatibility barrier for interspecific hybridization, post-zygotic incompatibility is common in interspecific pear hybrids. ...
Pear scab is a major disease of pear worldwide and is caused by two distinct species that are aligned with different commercial Pyrus species: Venturia pirina with European pear (P. communis) and V. nashicola with Asian pear species P. pyrifolia, P. ussuriensis and P. X bretschneideri. As these host-pathogen systems are mutually exclusive, interspecific pear breeding provides an avenue for breeding new scab-resistant cultivars. Here we describe the genetic mapping of resistance to V. nashicola in a pear progeny between interspecific pear selection P019R045T042 and ‘Shinko’ (P. pyrifolia) consisting of 274 seedlings, which was phenotyped twice with V. nashicola inoculum prepared from scab-infected leaves collected from trees of susceptible ‘Niitaka’ (P. pyrifolia). A set of 613 polymorphic DNA markers were selected from the apple and pear Illumina Infinium® II 9K single nucleotide polymorphism array and genotyping-by-sequencing for the creation of the parental genetic maps with JoinMap v4.1. Using the Interval Mapping module in MapQTL v6.0 software, two significant quantitative trait loci were detected in P019R045T042: one on linkage group (LG) 7 and another on LG10, which we name Rvn5 and Rvn6, respectively. Both Rvn5 and Rvn6 displayed weak additive effects for pear scab (V. nashicola) resistance when both loci worked together in this family. They will contribute to more strong resistance based on gene pyramiding through marker-assisted selections for the introduction of non-host resistance into both Asian and European pears through interspecific hybridization.
... The upper and lower parts on chromosome 13 were shown to be inherited from both parents, respectively, possibly due to the crossover of the pollen parent during gametogenesis. Genomic and genetic approaches would shed light on the underlining mechanism (Montanari et al. 2016). ...
Wide hybridizations across species and genera have been employed to enhance agriculturally important traits in crops. Within the tribe Maleae of the Rosaceae family, different genera and species exhibit several traits useful for increasing diversity and gene pool through hybridization. This study aimed to develop and characterize intergeneric hybrid individuals between Malus and Pyrus. Through seed germination, shoot multiplication, and rooting in vitro, acclimatized seedlings showing vegetative growth on their own roots were obtained from crosses of Malus × domestica pollinated by Pyrus communis, P. bretschneideri, and the Pyrus interspecific hybrid (P. communis × P. pyrifolia). Comparative analysis of leaf morphology, flow cytometry, and molecular genotyping confirmed the hybrid status of the individuals. Genome-wide genotyping revealed that all the hybrid individuals inherited genomic fragments symmetrically from the Malus and Pyrus parents. To the best of our knowledge, this is the first report on the development of intergeneric hybrid seedlings between Malus × domestica and P. bretschneideri. Furthermore, the Pyrus interspecific hybrid individual served as a bridge plant for introducing the genetic background of P. pyrifolia into Malus × domestica. The results of this study provided a crucial foundation for breeding through intergeneric hybridization between Malus and Pyrus, facilitating the incorporation of valuable traits from diverse gene pools.
... A typical example of postmating-prezygotic barriers is the cross-incompatibility between pollen and pistils [4][5][6][7][8][9][10][11]. Postzygotic barriers include hybrid seed abortion [4,, hybrid weaknesses [37][38][39][40][41][42][43][44][45][46][47], hybrid lethality [32,[48][49][50][51][52][53][54][55][56][57][58][59][60] or necrosis [61][62][63][64][65][66][67][68][69][70][71], and hybrid sterility [72][73][74][75][76][77][78][79] in plants of the F 1 generation, and hybrid breakdown is expressed as weaknesses, lethality, or sterility in plants of F 2 or later generations [49, [80][81][82][83][84][85][86][87][88][89]. Methods to overcome or bypass reproductive isolation are in demand for successful wide hybridization breeding [32]. ...
Hybrid lethality, a type of postzygotic reproductive isolation, is an obstacle to wide hybridization breeding. Here, we report the hybrid lethality that was observed in crosses between the cultivated tobacco, Nicotiana tabacum (section Nicotiana), and the wild tobacco species, Nicotiana simulans (section Suaveolentes). Reciprocal hybrid seedlings were inviable at 28 °C, and the lethality was characterized by browning of the hypocotyl and roots, suggesting that hybrid lethality is due to the interaction of nuclear genomes derived from each parental species, and not to a cytoplasmic effect. Hybrid lethality was temperature-sensitive and suppressed at 36 °C. However, when hybrid seedlings cultured at 36 °C were transferred to 28 °C, all of them showed hybrid lethality. After crossing between an N. tabacum monosomic line missing one copy of the Q chromosome and N. simulans, hybrid seedlings with or without the Q chromosome were inviable and viable, respectively. These results indicated that gene(s) on the Q chromosome are responsible for hybrid lethality and also suggested that N. simulans has the same allele at the Hybrid Lethality A1 (HLA1) locus responsible for hybrid lethality as other species in the section Suaveolentes. Haplotype analysis around the HLA1 locus suggested that there are at least six and two haplotypes containing Hla1-1 and hla1-2 alleles, respectively, in the section Suaveolentes.
... In the prezygotic type, the incompatible reaction usually involves the failure of pollen germination on the stigma, inferior pollen tube growth within pistils, and inhibition of pollen tube entry at the ovary (Moyle et al., 2014). In contrast, in the postzygotic type, the incompatible reaction occurs in various tissues and stages, from early embryonic development to the initial growth of seedlings and the reproductive stages of the resulting progeny (Bikard et al., 2009;Bomblies et al., 2007;Yamamoto et al., 2010;Montanari et al., 2016). Understanding cross-compatibility and the underlying mechanisms of hybridization barriers between species is indispensable for developing new hybrid crops with desirable traits. ...
Hybridization across species and genus has been utilized to improve agriculturally important traits in crops. These interspecific and intergeneric hybridizations are often inhibited by reproductive barriers at the prezygotic and postzygotic stages. In this study, we used intergeneric hybridization between apple and pear to investigate the effects of species and varietal differences on pollen tube growth, seed germination, and seedling survival in a wide range of germplasms. In apple pistils pollinated by pears, inferior pollen tube growth was often observed for European pear cultivars, whereas hybrid seedlings derived from a cross between apple and European pear showed higher survival rate. In contrast, Japanese pear and Chinese pear pollination resulted in higher fruit setting which likely resulted from a higher rate of compatible pistils but a lower rate of seedling survival. Our results suggest the presence of both prezygotic and postzygotic barriers that occur independently in different crossing combinations. We also developed a Cleaved Amplified Polymorphic Sequence marker for detecting intergeneric hybrids derived from a wide range of crosses between apples and pears. The results of the present study will help in the development of intergeneric hybrids between apple and pear for introducing valuable traits from a diverse gene pool.
... The candidate region corresponds to an approximate 240-kb region of the peach genome, where RLKs and genes with LRR were concentrated. The mapping of inter-specific reproductive barriers was also reported in other Rosaceae species (inter-specific pear: Montanari et al. 2016, apple × pear: Morimoto et al. 2020. Interestingly, lethal quantitative trait loci were located in the region with clusters of pest resistance genes in the inter-specific pear hybrid (Montanari et al. 2016). ...
... The mapping of inter-specific reproductive barriers was also reported in other Rosaceae species (inter-specific pear: Montanari et al. 2016, apple × pear: Morimoto et al. 2020. Interestingly, lethal quantitative trait loci were located in the region with clusters of pest resistance genes in the inter-specific pear hybrid (Montanari et al. 2016). From these results, the NB-LRR-mediated mechanism of hybrid incompatibility also exists in woody species as in herbal plants. ...
Knowledge of post-zygotic hybrid incompatibility is essential to understand speciation. Although the genes and molecular mechanisms involved in hybrid incompatibility are being elucidated in model plants and crops, the information on woody non-model plants is lacking. In the seedlings of a cross between the most famous ornamental cherry cultivar Cerasus × yedoensis ‘Somei-yoshino’ and its closely related wild species Cerasus itosakura, we discovered a hybrid incompatibility characterized by a phenotype in which growth stops after the expansion of the first true leaves and the seedling eventually dies. To elucidate the molecular mechanisms related to this seedling necrosis, we performed a comprehensive expressed gene analysis on normal-growth and necrotic weak-growth (SW) hybrid seedlings. The RNA-seq results showed over 1500 differentially expressed genes (DEGs) specified for the SW. Numerous genes associated with plant defense response, such as pathogenesis-related genes, and several receptor-like protein kinases were included in SW-specific upregulated DEGs. The Gene Ontology enrichment analysis also showed the significant association of “defense response” in SW seedlings. These upregulated defense-related gene expressions were particularly observed in the hypocotyls. On the contrary, the reduction of photosynthesis-related gene expression and reduction in the gene expressions of cell division and cell cycle at specific parts of seedlings were also observed in the SW. Our results suggest that an upregulated defense-related gene expression suppresses the meristem growth and deviation, resulting in growth failure as an autoimmune response in hybrid cherry seedlings.
... HI is a class of postzygotic isolating barriers found in both plants and animals that cause developmental difficulties, with full or partial lethality in the hybrid progenies (Coyne and Orr 2004). While many examples of reproductive isolation in native plant taxa were reported (Baack et al. 2015), inviability of interspecific F 1 or F 2 hybrid progenies of several important crops was well documented, e.g., rice (Chen et al. 2014), wheat (Mizuno et al. 2010), rye (Ren and Lelley 1988), potato (Valkonen and Watanabe 1999), tomato (Krüger et al. 2002), tobacco (Mino et al. 2002;Tezuka et al. 2010), cotton (Deng et al. 2019), apple (Schuster 2000), pear (Montanari et al. 2016), and grapes (Filler et al. 1994). Consequently, HI poses a major obstacle to wide hybridization and introgression breeding programs in agronomically important plants. ...
Reproductive isolation poses a major
obstacle to wide hybridization and introgression
breeding of plants. Hybrid inviability in the postzygotic
isolation barrier inevitably reduces hybrid fitness,
consequently causing hindrances in the establishment
of novel genotypes from the hybrids among
genetically divergent parents. The idea that the plant
immune system is involved in the hybrid problem is
applicable to the intra- and/or interspecific hybrids
of many different taxa. The lethality characteristics
and expression profile of genes associated with the
hypersensitive response of the hybrids, along with the
suppression of causative genes, support the deleterious
epistatic interaction of parental NB-LRR protein
genes, resulting in aberrant hyper-immunity reactions
in the hybrid. Moreover, the cellular, physiological,
and biochemical reactions observed in hybrid cells
also corroborate this hypothesis. However, the difference
in genetic backgrounds of the respective hybrids
may contribute to variations in lethality phenotypes
among the parental species combinations. The mixed state in parental components of the chaperone complex
(HSP90-SGT1-RAR1) in the hybrid may also
affect the hybrid inviability. This review article discusses
the facts and hypothesis regarding hybrid inviability,
alongside the findings of studies on the hybrid
lethality of interspecific hybrids of the genus Nicotiana.
A possible solution for averting the hybrid problem
has also been scrutinized with the aim of improving
the wide hybridization and introgression breeding
program in plants.
... The BDM model suggests that as ancestral species diverge, each lineage evolves mutations that are not harmful in their native genome, but interact negatively in a hybrid when two divergent genomes recombine (Bomblies, 2006). Hybrid lethality is induced by these deleterious epistatic interactions, which result in spontaneous activation of plant defense genes, primarily nucleotidebinding site leucine-rich repeat (NB-LRR) type resistance proteins Deng et al., 2019;Jeuken et al., 2009;Montanari et al., 2016). ...
... Our results demonstrate that postzygotic incompatibilities of F1 intergeneric Malinae hybrids resemble cases previously reported Montanari et al., 2016). Controlled pollinations provide important insights into intergeneric hybridization among A. melanocarpa, P. communis, and ·S. ...
... Observing varying degrees of hybrid necrosis is not an unusual biological phenomenon and has been observed in other cases. Montanari et al. (2016) were able to classify seedlings into different phenotypic classes of hybrid necrosis. Similarly, we classified A. melanocarpa · P. communis hybrids into early-stage hybrid necrosis and ·S. ...
Intergeneric hybridization between Aronia and Pyrus may provide a pathway for developing novel fruit types with larger, sweeter fruits, while maintaining the high levels of biologically health-promoting compounds present in Aronia fruits. Here we describe a deleterious genetic incompatibility, known as hybrid necrosis or hybrid lethality, that occurs in intergeneric F1 hybrids of Aronia melanocarpa x Pyrus communis and × Sorbaronia dippelii x Pyrus communis . Pollination experiments revealed that maternal A. melanocarpa and × S. dippelii pistils are compatible with pollen from P. communis . Controlled pollinations using different mating combinations resulted in varying levels of fruit and seed set. Because every combination produced at least some viable seeds, prezygotic incompatibility does not appear to be present. We attempted to recover putative intergeneric progeny via either in vitro germination or in vitro shoot organogenesis from cotyledons. Progeny of putative hybrids from A. melanocarpa x P. communis only survived for a maximum of 14 days before succumbing to hybrid lethality. Regeneration of × S. dippelii x P. communis was successful for two seedlings that have been maintained for an extended time in tissue culture. These two seedlings have leaf morphologies intermediate between the two parental genotypes. We also confirmed their hybrid status by using AFLPs and flow cytometry. Putative intergeneric hybrids were grown out ex vitro before showing symptoms of hybrid necrosis and dying after 3 months. Eventually micrografts failed, ultimately showing the same symptoms of hybrid necrosis. These results show that intergeneric hybridization is possible between Aronia and related genera in the Rosaceae, but there are postzygotic barriers to hybridity that can prevent the normal growth and development of the progeny.
... However, these are generally inhibited by both prezygotic and postzygotic barriers (Innoue et al. 2003;Morimoto et al. 2019). Recently, genetic loci controlling hybrid necrosis, which is one of the remarkable features of postzygotic barriers, was identified in the subtribe Malinae (Montanari et al. 2016) and the genus Prunus (Tsuruta and Mukai 2015). However, the genetic factors responsible for prezygotic barriers among Rosaceae species have not been characterized. ...
... Recently, Montanari et al. (2016) reported postzygotic hybrid necrosis in an interspecific pear population from a cross between P. bretschneideri and P. communis, and detected distorted segregation loci on seven linkage groups (LG), of which marker genotype on LG5 was associated with hybrid necrosis phenotype. Based on marker allele frequency, the lethal gene was predicted to be located around SSR marker Hi04d02 (Montanari et al. 2016), the similar region for Malus-Pyrus intergeneric barrier (Fig. 4b). ...
... Recently, Montanari et al. (2016) reported postzygotic hybrid necrosis in an interspecific pear population from a cross between P. bretschneideri and P. communis, and detected distorted segregation loci on seven linkage groups (LG), of which marker genotype on LG5 was associated with hybrid necrosis phenotype. Based on marker allele frequency, the lethal gene was predicted to be located around SSR marker Hi04d02 (Montanari et al. 2016), the similar region for Malus-Pyrus intergeneric barrier (Fig. 4b). Although, they suggested the observed segregation distortion could occur due to both prezygotic (not characterized in their study) and postzygotic stages, co-localization of the causal loci in both studies might implied that chromosome 5 is responsible for the establishment of species barrier at pre-and postzygotic stages in subtribe Malinae. ...
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.
... The partially homologous blocks on pseudo-chromosomes 1 and 7 may be the reason that a large number of markers that should have been mapped onto LG7 in the BD map were instead mapped onto LG1 [1,6,23]. However, the failure to anchor more scaffolds onto pseudo-chromosome 1 may also be related to the small size of the population that was used to construct the BD map, as well as lethal genes present in chromosome 1, which can cause interspecific hybrid necrosis [44]. ...
Background
Chromosomal level reference genomes provide a crucial foundation for genomics research such as genome-wide association studies (GWAS) and whole genome selection. The chromosomal-level sequences of both the European (Pyrus communis) and Chinese (P. bretschneideri) pear genomes have not been published in public databases so far.
Results
To anchor the scaffolds of P. bretschneideri ‘DangshanSuli’ (DS) v1.0 genome into pseudo-chromosomes, two genetic maps (MH and YM maps) were constructed using half sibling populations of Chinese pear crosses, ‘Mantianhong’ (MTH) × ‘Hongxiangsu’ (HXS) and ‘Yuluxiang’ (YLX) × MTH, from 345 and 162 seedlings, respectively, which were prepared for SNP discovery using genotyping-by-sequencing (GBS) technology. The MH and YM maps, each with 17 linkage groups (LGs), were constructed from 2606 and 2489 SNP markers and spanned 1847 and 1668 cM, respectively, with average marker intervals of 0.7. The two maps were further merged with a previously published genetic map (BD) based on the cross ‘Bayuehong’ (BYH) × ‘Dangshansuli’ (DS) to build a new integrated MH-YM-BD map. By using 7757 markers located on the integrated MH-YM-BD map, 898 scaffolds (400.57 Mb) of the DS v1.0 assembly were successfully anchored into 17 pseudo-chromosomes, accounting for 78.8% of the assembled genome size. About 88.31% of them (793 scaffolds) were directionally anchored with two or more markers on the pseudo-chromosomes. Furthermore, the errors in each pseudo-chromosome (especially 1, 5, 7 and 11) were manually corrected and pseudo-chromosomes 1, 5 and 7 were extended by adding 19, 12 and 14 scaffolds respectively in the newly constructed DS v1.1 genome. Synteny analyses revealed that the DS v1.1 genome had high collinearity with the apple genome, and the homologous fragments between pseudo-chromosomes were similar to those found in previous studies. Moreover, the red-skin trait of Asian pear was mapped to an identical locus as identified previously.
Conclusions
The accuracy of DS v1.1 genome was improved by using larger mapping populations and merged genetic map. With more than 400 MB anchored to 17 pseudo-chromosomes, the new DS v1.1 genome provides a critical tool that is essential for studies of pear genetics, genomics and molecular breeding.
Electronic supplementary material
The online version of this article (10.1186/s12864-018-5224-6) contains supplementary material, which is available to authorized users.
... This confirms the results of Shaw et al. (2004) that indicated significant differences among the six clones tested in egg numbers per square metre of leaf and also egg numbers for the whole-plant counts for individual selections, where results ranged from 52 to 327, compared with 264 on 'Bartlett'. The QTL identified for pear slug leaf damage on LG9 of 'Moonglow' was on a different linkage group from those found for pear psylla antibiosis in the same family by Montanari et al. (2016a), which were identified on LG15 for 'Moonglow' and LG5, LG8 and ...
... LG11 for 'PremP003', and those found on LG1, LG4 and LG17 by Perchepied et al. (2016) which were identified from Pyrus ussuriensis derivatives. The QTLs found for pear slug for oviposition antixenosis in this study were also found on different linkage groups from those found for psylla antibiosis by Montanari et al. (2016a) and Perchepied et al. (2016). ...
... Whilst LG9 of 'Moonglow' and LG10 of 'PremP003' were largely distorted (Montanari et al. 2016a), this did not appear to have affected the genetic mapping of the pear slug/sawfly resistance, but an enlarged family would have enabled a more precise mapping of the QTLs. This also might have brought the pear slug damage QTL on LG9 of 'Moonglow' closer to the sawfly oviposition antixenosis QTL, as the amount of leaf damage may have been a function of both the number of sawfly eggs deposited on the leaves and an antibiosis effect of leaf feeding on pear slug. ...
Whilst minor pests of pear, both sawfly larvae (pear slug) and pear blister mite can at times cause sufficient damage in commercial and particularly in organic pear production for treatment to be required. In the course of breeding new pear cultivars, resistance to both pests was identified in an interspecific pear family raised from a cross between ‘PremP003’ and ‘Moonglow’. The replicated seedling family was subjected to uninhibited insect development for both pests in an insect-proof cage, providing ample infestations for resistance segregation. Using an existing genetic map for the family, one major quantitative trait locus (QTL) for resistance to pear blister mite was located to linkage group 13 (LG13) of ‘PremP003’. For pear slug, we mapped three QTLs for oviposition antixenosis, one each on LG7 and LG9 of ‘Moonglow’ and another on LG10 of ‘PremP003’, and one resistance QTL for leaf damage to LG9 of ‘Moonglow’ at a distance of 8.1 cM below the oviposition QTL. Incorporating these resistances into future cultivars could contribute to a reduction in pesticide use in pear production, especially in combination with the resistances for pear psylla (Cacopsylla pyri) and fire blight (Erwinia amylovora) recently mapped in the same population using marker-assisted selection.
