Allopolyploidization in Cucumis contributes to delayed leaf maturation with repression of redundant homoeologous genes

Abstract

The important role of polyploidy in plant evolution is widely recognized. However, many questions remain to be explored to address how polyploidy affects the phenotype of the plant. To shed light on the phenotypic and molecular impacts of allopolyploidy, we investigated the leaf development of a synthesized allotetraploid (Cucumis × hytivus), with an emphasis on chlorophyll development. Delayed leaf maturation was identified in C. × hytivus, based on delayed leaf expansion, initial chlorophyll deficiency in the leaves and disordered sink-source transition. Anatomical observations also revealed disturbed chloroplast development in C. ×hytivus. The determination of chlorophyll biosynthesis intermediates suggested that the chlorophyll biosynthesis pathway of C. × hytivus is blocked at the site at which uroporphyrinogen III is catalysed to coproporphyrinogen III. Three chlorophyll biosynthesis-related genes, HEMA1, HEME2 and POR, were significantly repressed in C. × hytivus. Sequence alignment showed both synonymous and non-synonymous substitutions in the HEMA1, HEME2 and POR genes of the parents. Cloning of the chlorophyll biosynthetic genes suggested the retention of homoeologs. In addition, a chimeric clone of the HEMA1 gene that consisted of homologous genes from the parents was identified in C. × hytivus. Overall, our results showed that allopolyploidization in Cucumis has resulted in disturbed chloroplast development and reduced chlorophyll biosynthesis caused by the repressed expression of duplicated homologous genes, which further led to delayed leaf maturation in the allotetraploid, C. × hytivus. The preferential retention/loss of certain types of genes and non-reciprocal homoeologous recombination were also supported in the present study, which provides new insights into the impact of allopolyploidy.

High-throughput sequencing reveals the change of microRNA expression caused by allopolyploidization in Cucumis

“…miR171 was reported to be crucial for regulating chlorophyll biosynthesis through the gene encoding protochlorophyllide oxidoreductase (POR) ). Recently we have identified chlorophyll deficiency and repression of chlorophyll biosynthesis genes, including the POR gene, in C. ×hytivus (Yu et al 2018). The results presented here prompts us to further investigate the mechanism of how miRNAs regulate the chlorophyll biosynthesis in the allopolyploids.…”

Whole‐Genome Sequence of Synthesized Allopolyploids in Cucumis Reveals Insights into the Genome Evolution of Allopolyploidization

“…It also supports our earlier AFLP analysis that some of the parental fragments lost at the hybrid stage reappeared after allopolyploid formation. [ 18d ] However, the underlying mechanism of regaining the lost gene needs to be further uncovered. Although bioinformatic inference of gene loss is widely applied in polyploid studies, it should also be noted that statistical false results, for example, false read alignment, are also possible, since the definition of gene loss is based on the artificially calculated threshold value.…”

“…×hytivus , which may contribute to the novel phenotypic variation found in amphidiploids, such as delayed leaf maturation. [ 18 ] However, understanding the underlying mechanisms has been limited by the lack of genomic information about this synthetic species. In the present study, several advanced technologies, including whole‐genome shotgun sequencing, single‐molecule real‐time (SMRT) sequencing, high‐throughput chromosome conformation capture (Hi‐C) technology, and BioNano optical genome mapping, were adopted to generate a high‐quality genome sequence of C .…”

Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid

“…Previous studies have indicated that almost all ancestors of seed plants have experienced at least one round of genome doubling [4,5]. Allopolyploidization often results in complex changes at different aspects, such as genomic changes including homoeologous exchanges and loss of genes [6,7,8], nonadditive gene expression [9,10], and changes in epigenetic modifications [5,11]. During allopolyploidization, not merely two different nuclear genomes combine, but also different sources of chloroplast and mitochondrial genomes interact in the same cell, in view of the complex interactions between the nuclear and organelle genomes [12].…”