Allopolyploids are often faced with the challenge of maintaining well-coordination between nuclear and cytoplasmic genes inherited from different species. The synthetic allotetraploid Cucumis × hytivus is a useful model to explore cytonuclear coevolution. In this study, the sequences and expression of cytonuclear enzyme complex RuBisCO as well as its content and activity in C. × hytivus were compared to its parents to explore plastid–nuclear coevolution. The plastome-coded rbcL gene sequence was confirmed to be stable maternal inheritance, and parental copy of nuclear rbcS genes were both preserved in C. × hytivus. Thus, the maternal plastid may interact with the biparentally inherited rbcS alleles. The expression of the rbcS gene of C-homoeologs (paternal) was significantly higher than that of H-homoeologs (maternal) in C. × hytivus (HHCC). Protein interaction prediction analysis showed that the rbcL protein has stronger binding affinity to the paternal copy of rbcS protein than that of maternal copy in C. × hytivus, which might explain the transcriptional bias of the rbcS homoeologs. Moreover, both the activity and content of RuBisCO in C. × hytivus showed mid-parent heterosis. In summary, our results indicate a paternal transcriptional bias of the rbcS genes in C. × hytivus, and we found new nuclear–cytoplasmic combination may be one of the reasons for allopolyploids heterosis.
The importance of allopolyploidy in plant evolution has been widely recognized. The genetic changes triggered by allopolyploidy, however, are not yet fully understood due to inconsistent phenomena reported across diverse species. The construction of synthetic polyploids offers a controlled approach to systematically reveal genomic changes that occur during the process of polyploidy. This study reports the first fully sequenced synthetic allopolyploid constructed from a cross between Cucumis sativus and C. hystrix, with high‐quality assembly. The two subgenomes are confidently partitioned and the C. sativus‐originated subgenome predominates over the C. hystrix‐originated subgenome, retaining more sequences and showing higher homeologous gene expression. Most of the genomic changes emerge immediately after interspecific hybridization. Analysis of a series of genome sequences from several generations (S0, S4–S13) of C. ×hytivus confirms that genomic changes occurred in the very first generations, subsequently slowing down as the process of diploidization is initiated. The duplicated genome of the allopolyploid with double genes from both parents broadens the genetic base of C. ×hytivus, resulting in enhanced phenotypic plasticity. This study provides novel insights into plant polyploid genome evolution and demonstrates a promising strategy for the development of a wide array of novel plant species and varieties through artificial polyploidization.
SUMMARY Karyotype dynamics driven by complex chromosome rearrangements constitute a fundamental issue in evolutionary genetics. The evolutionary events underlying karyotype diversity within plant genera, however, have rarely been reconstructed from a computed ancestral progenitor. Here, we developed a method to rapidly and accurately represent extant karyotypes with the genus, Cucumis, using highly customizable comparative oligo‐painting (COP) allowing visualization of fine‐scale genome structures of eight Cucumis species from both African‐origin and Asian‐origin clades. Based on COP data, an evolutionary framework containing a genus‐level ancestral karyotype was reconstructed, allowing elucidation of the evolutionary events that account for the origin of these diverse genomes within Cucumis. Our results characterize the cryptic rearrangement hotspots on ancestral chromosomes, and demonstrate that the ancestral Cucumis karyotype (n = 12) evolved to extant Cucumis genomes by hybridizations and frequent lineage‐ and species‐specific genome reshuffling. Relative to the African species, the Asian species, including melon (Cucumis melo, n = 12), Cucumis hystrix (n = 12) and cucumber (Cucumis sativus, n = 7), had highly shuffled genomes caused by large‐scale inversions, centromere repositioning and chromothripsis‐like rearrangement. The deduced reconstructed ancestral karyotype for the genus allowed us to propose evolutionary trajectories and specific events underlying the origin of these Cucumis species. Our findings highlight that the partitioned evolutionary plasticity of Cucumis karyotype is primarily located in the centromere‐proximal regions marked by rearrangement hotspots, which can potentially serve as a reservoir for chromosome evolution due to their fragility.
GATA transcription factors are a class of transcriptional regulatory proteins that contain a characteristic type-IV zinc finger DNA-binding domain, which play important roles in plant growth and development. The GATA gene family has been characterized in various plant species. However, GATA family genes have not been identified in cucumber. In this study, 26 GATA family genes were identified in cucumber genome, whose physicochemical characteristics, chromosomal distributions, phylogenetic tree, gene structures conserved motifs, cis-regulatory elements in promoters, homologous gene pairs, downstream target genes were analyzed. Tissue expression profiles of cucumber GATA family genes exhibited that 17 GATA genes showed constitutive expression, and some GATA genes showed tissue-specific expression patterns. RNA-seq analysis of green and virescent leaves revealed that seven GATA genes might be involved in the chloroplast development and chlorophyll biosynthesis. Importantly, expression patterns analysis of GATA genes in response to abiotic and biotic stresses indicated that some GATA genes respond to either abiotic stress or biotic stress, some GATA genes such as Csa2G162660, Csa3G017200, Csa3G165640, Csa4G646060, Csa5G622830 and Csa6G312540 were simultaneously functional in resistance to abiotic and biotic stresses. Overall, this study will provide useful information for further analysis of the biological functions of GATA factors in cucumber.
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