Differential alternative polyadenylation contributes to the developmental divergence between two rice subspecies, japonica and indica

Abstract

Alternative polyadenylation (APA) is a widespread post-transcriptional mechanism that regulates gene expression through mRNA metabolism, playing a pivotal role in modulating phenotypic traits in rice (Oryza sativa L.). However, little is known about the APA-mediated regulation underlying the distinct characteristics between two major rice subspecies, indica and japonica. Using a poly(A)-tag sequencing approach, polyadenylation (poly(A)) site profiles were investigated and compared pairwise from germination to the mature stage between indica and japonica, and extensive differentiation in APA profiles was detected genome-wide. Genes with subspecies-specific poly(A) sites were found to contribute to subspecies characteristics, particularly in disease resistance of indica and cold-stress tolerance of japonica. In most tissues, differential usage of APA sites exhibited an apparent impact on the gene expression profiles between subspecies, and genes with those APA sites were significantly enriched in quantitative trait loci (QTL) related to yield traits, such as spikelet number and 1000-seed weight. In leaves of the booting stage, APA site-switching genes displayed global shortening of 3 0 untranslated regions with increased expression in indica compared with japonica, and they were overrepresented in the porphyrin and chlorophyll metabolism pathways. This phenomenon may lead to a higher chlorophyll content and photosynthesis in indica than in japonica, being associated with their differential growth rates and yield potentials. We further constructed an online resource for querying and visualizing the poly(A) atlas in these two rice subspecies. Our results suggest that APA may be largely involved in developmental differentiations between two rice subspecies, especially in leaf characteristics and the stress response, broadening our knowledge of the post-transcriptional genetic basis underlying the divergence of rice traits.

PlantAPAdb: A Comprehensive Database for Alternative Polyadenylation Sites in Plants

“…All queries except for the sample-centric search will lead to a media page that shows the number of PACs in each species. Take the Yellow-Green Leaf8 (YGL8) gene, for example, which has been reported to have a strong impact on chlorophyll content and photosynthesis in rice (Zhou et al, 2019). This gene has multiple poly(A) sites and exhibits 39 UTR APA site switching between two rice subspecies (Zhou et al, 2019).…”

“…Take the Yellow-Green Leaf8 (YGL8) gene, for example, which has been reported to have a strong impact on chlorophyll content and photosynthesis in rice (Zhou et al, 2019). This gene has multiple poly(A) sites and exhibits 39 UTR APA site switching between two rice subspecies (Zhou et al, 2019). Users can directly search for YGL8 and then select Oryza sativa Japonica Group from the search result page (Fig.…”

“…APA is also prevalent in plants. For example, 55% of genes in moso bamboo (Phyllostachys edulis; Wang et al, 2017), more than 60% of genes in Medicago truncatula (Wu et al, 2014), and ;70% of genes in Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa) undergo APA (Shen et al, 2008a(Shen et al, , 2011Wu et al, 2011;Fu et al, 2016;Zhou et al, 2019). An increasing body of evidence has indicated that APA is dynamically modulated in a developmental, tissue-specific, or environmentally responsive manner.…”

“…Shorter 39 UTRs that escape regulation by 39 UTR elements, such as microRNA-binding sites, AU-rich elements, and GU-rich elements, may be more stable than their corresponding longer 39 UTRs and result in the production of more protein (Mayr and Bartel, 2009;Mayr, 2017). In plants, APA has been demonstrated in the regulation of genes that are involved in processes such as flowering time control, amino acid biosynthesis, plant incompatibility, and oxidative stress responses (Thomas et al, 2012;Lin et al, 2017;Hong et al, 2018;Fu et al, 2019;Zhou et al, 2019). Given the importance of APA for gene expression and cellular function as well as the rapid accumulation of APA sites in diverse species, it is necessary that we have a comprehensive and easily accessible catalog of poly(A) sites with quantified expression levels on a genome-wide scale.…”

Expanding the Coverage of the Metabolic Landscape in Cultivated Rice with Integrated Computational Approaches

“…Rice ( Oryza sativa L.) is one of the major staple foods worldwide, and it is critical to explore its chemical compositions and metabolic traits for the enhancement of grains quality and nutritional value [21, 22]. The two major subspecies of cultivated rice, indica and japonica , formed during domestication, display distinct features in morphology and physiology [23-25]. In recent years, a series of studies on rice metabolomics were performed, which provides the foundation for the metabolic components of rice [2, 5, 26, 27].…”