Traversing the effects of ploidy changes in different Eragrostis curvula genotypes through high‐throughput RNA sequencing

TL;DR

This study explores how extra chromosome sets in Eragrostis curvula grass affect gene activity, revealing trade-offs between stress tolerance and forage quality.

Contribution

The study identifies ploidy-sensitive genes and their roles in stress tolerance and biomass digestibility in Eragrostis curvula.

Findings

Higher ploidy levels in Eragrostis curvula are linked to increased stress tolerance and changes in cell wall and lignin-related genes.

A trade-off between stress tolerance and forage digestibility is observed at higher ploidy levels.

Ploidy-sensitive genes and transcriptional networks suggest a rewiring of gene regulation with increasing chromosome sets.

Abstract

Polyploidization has played a key role in plant genome evolution. Eragrostis curvula (Schrad.) Ness, a perennial forage grass species of the Poaceae family, is an excellent model for investigating genome duplication due to its natural variation in ploidy levels. To explore the transcriptomic consequences of polyploidy, we performed high‐throughput RNA‐Seq on leaf tissue from 10 E. curvula genotypes ranging from diploid to octoploid. Differential expression analyses revealed that the number of differentially expressed genes increased with increasing ploidy, suggesting a rewiring of the gene regulatory network. Several putative genes associated with stress tolerance and epigenetic regulation were modulated at higher ploidy levels. Forage digestibility and saccharification efficiency were likely altered at higher ploidy levels, mainly due to the upregulation of putative genes involved in lignin biosynthesis, cell wall remodeling, and polysaccharide metabolism. Our results may reveal a fine‐tuning regulation favoring stress tolerance over forage digestibility. The analysis of the core set of 433 Ploidy_vs_2x DEGs, consistently expressed in a polyploidy‐sensitive manner, revealed upregulation of genes involved in the ubiquitination pathway, stress response, cell wall remodeling, hormonal regulation, and terpenoid biosynthesis. Ploidy‐dependent transcriptional responses were also observed in the patterns of transcription factor families, underlining a different reprogramming of the transcriptional network at each ploidy level. An integrated network‐based approach combining WGCNA and SWIM (SWItchMiner) identified a predicted master regulator target gene putatively associated with increased forage digestibility. Our findings provide valuable insights into the molecular mechanisms underlying polyploidization in E. curvula, with implications for breeding strategies to balance stress tolerance and biomass digestibility.

Ploidy‐sensitive genes were uniquely identified at each ploidy level in Eragrostis curvula genotypes.Novelty at the cellular level might be generated by increasing ploidy levels.Ploidy‐dependent variation in the E. curvula transcriptomic landscape reflects both effects of genome duplication and the genetic background of each genotype.Co‐expression network analysis underlined the involvement of putative genes associated with lignin biosynthesis, cell wall remodeling, epigenetic regulation, and stress responses at higher ploidy levels.A trade‐off between increased stress tolerance and reduced forage digestibility likely occurred at higher ploidy levels.This study provides genomic resources for future functional genetic studies aimed at balancing stress tolerance and improving biomass digestibility.

Ploidy‐sensitive genes were uniquely identified at each ploidy level in Eragrostis curvula genotypes.

Novelty at the cellular level might be generated by increasing ploidy levels.

Ploidy‐dependent variation in the E. curvula transcriptomic landscape reflects both effects of genome duplication and the genetic background of each genotype.

Co‐expression network analysis underlined the involvement of putative genes associated with lignin biosynthesis, cell wall remodeling, epigenetic regulation, and stress responses at higher ploidy levels.

A trade‐off between increased stress tolerance and reduced forage digestibility likely occurred at higher ploidy levels.

This study provides genomic resources for future functional genetic studies aimed at balancing stress tolerance and improving biomass digestibility.

Many crop species carry extra sets of chromosomes (polyploidy), which can generate novelty at the cellular level. Our study investigated the transcriptomic effects of genome doubling in Eragrostis curvula, a forage grass that naturally occurs with two to eight sets of chromosomes. Using an RNA sequencing approach, we searched for genes associated with the transition from diploid to polyploid. Many genes related to stress responses, cell wall reprogramming, and epigenetic regulation were modulated upon genome duplication in E. curvula. We identified candidate genes that could provide a polyploid advantage under climate change fluctuations while improving forage digestibility. These genes can be used as targets of breeding programs aimed at balancing stress tolerance and biomass digestibility. Overall, our findings show how having extra chromosome sets can generate useful crop diversity, laying the basis for developing more resilient, high‐quality forage grasses.

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