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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 (S 0 , S 4 -S 13 ) 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., Competing Interests: The authors declare no conflict of interest., (© 2021 The Authors. Advanced Science published by Wiley‐VCH GmbH.)

Long non-coding RNAs (lncRNAs) play critical regulatory roles in various biological processes. However, the presence of lncRNAs and how they function in plant polyploidy are still largely unknown. Hence, we examined the profile of lncRNAs in a nascent allotetraploid Cucumis hytivus (S 14 ), its diploid parents, and the F 1 hybrid, to reveal the function of lncRNAs in plant-interspecific hybridization and whole genome duplication. Results showed that 2206 lncRNAs evenly transcribed from all 19 chromosomes were identified in C. hytivus , 44.6% of which were from intergenic regions. Based on the expression trend in allopolyploidization, we found that a high proportion of lncRNAs (94.6%) showed up-regulated expression to varying degrees following hybridization. However, few lncRNAs (33, 2.1%) were non-additively expressed after genome duplication, suggesting the significant effect of hybridization on lncRNAs, rather than genome duplication. Furthermore, 253 cis-regulated target genes were predicted for these differentially expressed lncRNAs in S 14 , which mainly participated in chloroplast biological regulation (e.g., chlorophyll synthesis and light harvesting system). Overall, this study provides new insight into the function of lncRNAs during the processes of hybridization and polyploidization in plant evolution.

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.

Studies have shown that polyploidy has pronounced effects on plants in multiple aspects, including genome structure, gene expression, metabolism and so on, which finally induce changes in phenotype. Many of these changes occurred immediately after polyploidization and retained or lost later. Therefore, it is meaningful for crop breeders to gain knowledge of these changes when it is relatively stable. In this study, we investigated the phenotypes of a highly self-pollinated synthesized allotetraploid in Cucumis, named with Cucumis × hytivus J. F. Chen & J. H. Kirkbr. (C. ×hytivus for short). Results showed that although many phenotypes of C. ×hytivus were intermediate between its parents, total leaf area and cell size exhibited parent-of-origin and dosage effect, respectively. Additionally, C. ×hytivus exhibited divergent biomass allocation strategy compared to the parents, developing more leaves. Beside the commonalities across different polyploid systems, the combination of hybridity and genome duplication in allopolyploids may lead to a diverse possibility of phenotypic changes. In spite of the reduced light absorption by less photosynthetic pigments in young leaves, allopolyploidy caused limited adverse effect on the photosynthesis of C. ×hytivus, which may benefit from the increased leaf thickness and potentially facilitated the survival and speciation of this novel species. The present study offers novel insights into the varied phenotypic effects of polyploidy and is a valuable reference for the crop improvement through polyploidization. [ABSTRACT FROM AUTHOR]