Chromosome‐scale reference genome provides insights into the genetic origin and grafting‐mediated stress tolerance of <i>Malus prunifolia</i>

Li, Zhong-xing; Wang, Lun; He, Jieqiang; Li, Xuewei; Hou, Nan; Guo, Junxing; Niu, Chundong; Li, Chaoshuo; Liu, Bo; Xu, Jidi; Xie, Yinpeng; Zou, Dehui; Shen, Xiaoxia; Lü, Lei; Geng, Dali; Chen, Pengxiang; Jiang, Lijuan; Wang, Liping; Li, Haiyan; Malnoy, Mickaël; Deng, Cecilia; Zou, Yangjun; Li, Cuiying; Zhan, Xiangqiang; Dong, Yang; Notaguchi, Michitaka; Feng-wang, MA; Xu, Qiang; Guan, Qingmei

doi:10.1111/pbi.13817

Cited by 17 publications

(17 citation statements)

References 4 publications

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“…In previous studies of annual and perennial plants, it has also been reported that heterologous cell interaction changed the genome-wide methylation profile of scions. After heterografting of Malus prunifolia ‘Fupingqiuzi’ and commercial apple ( M. × domestica ‘Golden Delicious’), the DNA methylation levels in CG and CHG of ‘Golden Delicious’ were significantly increased [ 6 ]. Similarly, interspecific heterografting of cucumber ( Cucumis sativus ) and melon ( Cucumis melo ) also resulted in increased DNA methylation in the scion [ 21 ].…”

Section: Discussionmentioning

confidence: 99%

“…[ 5 ] found that DNA methylation can be mediated by mobile small RNAs in grafts. In fruit trees heterologous rootstocks can induce genome-wide DNA methylation variation in scions, thereby imparting resistance [ 6 , 7 ]. In vegetables, after grafting with different rootstocks, the eggplant scion undergoes demethylation, which induces changes in vigor [ 8 ].…”

Section: Introductionmentioning

confidence: 99%

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The role of DNA methylation in the maintenance of phenotypic variation induced by grafting chimerism inBrassica

Liu

Wang

Xiao

et al. 2023

Horticulture Research

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Grafting facilitates the interaction between heterologous cells with different genomes, resulting in abundant phenotypic variation, which provides opportunities for crop improvement. However, how grafting-induced variation occurs and is transmitted to progeny remain elusive. Grafting chimera, especially periclinal chimera, which has genetically distinct cell layers throughout the plant, is an excellent model to probe the molecular mechanisms of grafting induced variation maintenance. Here, we regenerated a plant from the T cell layer of a periclinal chimera TCC (where the apical meristem was artificially divided into three cell layers from outside to inside, L1-L2-L3; T = tuber mustard, C = red cabbage), named rTTT0 (r = regenerated). Compared with the control (rsTTT, s = self-grafted), rTTT0 had multiple phenotypic variations, especially leaf shape variation, which could be maintained in sexual progeny. Transcriptomes were analyzed and 58 phenotypic variations associated genes were identified. Whole-genome bisulfite sequencing analyses revealed that the methylome of rTTT0 was changed, and the CG methylation level was significantly increased by 8.74%. In rTTT0, the coding gene bodies are hypermethylated in the CG context, while their promoter regions are hypomethylated in the non-CG context. DNA methylation changes in the leaf shape variation-associated coding genes, ARF10, IAA20, ROF1 and TPR2, were maintained for five generations of rTTT0. Interestingly, graft chimera also affected transcription of the microRNA gene (MIR), in which the DNA methylation levels of the promoter of 3 MIRs associated with leaf shape variation were changed in rTTT0, and the DNA methylation modification of MIR319 was maintained to the fifth generation of selfed progeny of rTTT0 (rTTT5). These findings demonstrate that DNA methylation of coding and non-coding genes plays an important role in heterologous cell interaction-induced variation formation and its transgenerational inheritance.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The role of DNA methylation in the maintenance of phenotypic variation induced by grafting chimerism inBrassica

Liu

Wang

Xiao

et al. 2023

Horticulture Research

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“…The native species M. prunifolia is a species of crabapple that is widely distributed in China and has been cultivated for more than 2000 years for the selection of excellent rootstock. M. prunifolia may be a hybrid between M. baccata and M. sieversii in Kazakhstan [ 43 , 50 ]. The grouping into CladeII and CladeIII suggests that M. domestica , M .sieversii , and M. prunifolia retain specialized functions in Central and East Asia, and the proteins encoded by these cyclophilin genes may be conserved overall but not shared with other Malus species.…”

Section: Discussionmentioning

confidence: 99%

“…Several genomes of the genus Malus have been published [43][44][45][46], and these have provided an important basis for systematic research. Here, we used the HMM strategy to search the cyclophilin family members of four other Malus species, Malus sieversii, Malus sylvestris, Malus baccata, and Malus prunifolia, and identified 26, 21, 24, and 18 cyclophilins, respectively (Supplementary Table 1).…”

Section: Phylogenetic Analysis Of Mdcypsmentioning

confidence: 99%

Genome-wide identification and stress response analysis of cyclophilin gene family in apple (Malus × domestica)

Qiao

Wang

et al. 2022

BMC Genomics

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Background Cyclophilin (CYP) belongs to the immunophilin family and has peptidyl-prolyl cis-trans isomerase (PPIase) activity, which catalyzes the cis-trans isomerization process of proline residues. CYPs widely exist in eukaryotes and prokaryotes, and contain a conserved cyclophilin-like domain (CLD). Plant cyclophilins are widely involved in a range of biological processes including stress response, metabolic regulation, and growth and development. Result In this study, 30 cyclophilin genes on 15 chromosomes were identified from the ‘Golden Delicious’ apple (M. domestica) genome. Phylogenetic analysis showed that the cyclophilin family genes can be divided into three clades in Malus. Collinear analysis showed that ten gene pairs were the result of segmental duplication. Analysis of gene and protein structure further supported the phylogenetic tree and collinearity analysis. The expression of MdCYPs in different organs was higher in leaves, flowers, and fruits. Ten and eight CYPs responded to drought and salt stress, respectively. MdCYP16, a nuclear-localized MD CYP, was screened from the intersection of the two expression profiling datasets and was highly sensitive to drought and salt stress. GUS staining of transgenic Arabidopsis indicated that MdCYP16 may be involved in the regulation of abiotic stress. Conclusion This study systematically analyzed members of the apple cyclophilin family and confirmed the involvement of MdCYP16 as a nuclear-localized MD cyclophilin that acts in response to salt and drought stress in apple. Our work identifies members of the apple cyclophilin gene family, and provides an important theoretical basis for in-depth study of cyclophilin function. Additionally, the analysis provides candidate genes that may be involved in stress response in apple.

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“…Public genetic resources in Malus species have increased in the last two decades, from the reference genomes for M. × domestica cv. 'Golden Delicious' (Velasco et al, 2010;Daccord et al, 2017) and 'Gala' (Sun et al, 2020) to sequencing of 'Gala' wild progenitors M. sieversii and M. sylvestris (Sun et al, 2020), as well as wild M. baccata and M. prunifolia (Chen et al, 2019;Li et al, 2022). Wild accessions with publicly available genome resources, however, accumulate exclusively (M. sieversii, M. sylvestris and M. baccata) or predominantly (M. prunifolia) phloridzin according to a previous study (Gutierrez et al, 2018b).…”

Section: Identification Of Candidate Genes Involved In Sieboldin Bios...mentioning

confidence: 99%

De novo transcriptome assembly and functional analysis reveal a dihydrochalcone 3-hydroxylase(DHC3H) of wild Malus species that produces sieboldin in vivo

et al. 2022

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Sieboldin is a specialised secondary metabolite of the group of dihydrochalcones (DHC), found in high concentrations only in some wild Malus species, closely related to the domesticated apple (Malus × domestica L.). To date, the first committed step towards the biosynthesis of sieboldin remains unknown. In this study, we combined transcriptomic analysis and a de novo transcriptome assembly to identify two putative 3-hydroxylases in two wild Malus species (Malus toringo (K. Koch) Carriere syn. sieboldii Rehder, Malus micromalus Makino) whose DHC profile is dominated by sieboldin. We assessed the in vivo activity of putative candidates to produce 3-hydroxyphloretin and sieboldin by de novo production in Saccharomyces cerevisiae. We found that CYP98A proteins of wild Malus accessions (CYP98A195, M. toringo and CYP98A196, M. micromalus) were able to produce 3-hydroxyphloretin, ultimately leading to sieboldin accumulation by co-expression with PGT2. CYP98A197-198 genes of M. × domestica, however, were unable to hydroxylate phloretin in vivo. CYP98A195-196 proteins exerting 3-hydroxylase activity co-localised with an endoplasmic reticulum marker. CYP98A protein model from wild accessions showed mutations in key residues close to the ligand pocket predicted using phloretin for protein docking modelling. These mutations are located within known substrate recognition sites of cytochrome P450s, which could explain the acceptance of phloretin in CYP98A protein of wild accessions. Screening a Malus germplasm collection by HRM marker analysis for CYP98A genes identified three clusters that correspond to the alleles of domesticated and wild species. Moreover, CYP98A isoforms identified in M. toringo and M. micromalus correlate with the accumulation of sieboldin in other wild and hybrid Malus genotypes. Taken together, we provide the first evidence of an enzyme producing sieboldin in vivo that could be involved in the key hydroxylation step towards the synthesis of sieboldin in Malus species.

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Chromosome‐scale reference genome provides insights into the genetic origin and grafting‐mediated stress tolerance of Malus prunifolia

Cited by 17 publications

References 4 publications

The role of DNA methylation in the maintenance of phenotypic variation induced by grafting chimerism inBrassica

The role of DNA methylation in the maintenance of phenotypic variation induced by grafting chimerism inBrassica

Genome-wide identification and stress response analysis of cyclophilin gene family in apple (Malus × domestica)

De novo transcriptome assembly and functional analysis reveal a dihydrochalcone 3-hydroxylase(DHC3H) of wild Malus species that produces sieboldin in vivo

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