Genome-Wide Identification of Cassava Serine/Arginine-Rich Proteins: Insights into Alternative Splicing of Pre-mRNAs and Response to Abiotic Stress

Abstract

Serine/arginine-rich (SR) proteins have an essential role in the splicing of pre-messenger RNA (pre-mRNA) in eukaryote. Pre-mRNA with introns can be alternatively spliced to generate multiple transcripts, thereby increasing adaptation to the external stress conditions in planta. However, pre-mRNA of SR proteins can also be alternatively spliced in different plant tissues and in response to diverse stress treatments, indicating that SR proteins might be involved in regulating plant development and adaptation to environmental changes. We identified and named 18 SR proteins in cassava and systematically studied their splicing and transcriptional changes under tissue-specific and abiotic stress conditions. Fifteen out of 18 SR genes showed alternative splicing in the tissues. 45 transcripts were found from 18 SR genes under normal conditions, whereas 55 transcripts were identified, and 21 transcripts were alternate spliced in some SR genes under salt stress, suggesting that SR proteins might participate in the plant adaptation to salt stress. We then found that overexpression of MeSR34 in Arabidopsis enhanced the tolerance to salt stress through maintaining reactive oxygen species homeostasis and increasing the expression of calcineurin B-like proteins (CBL)–CBL-interacting protein kinases and osmotic stress-related genes. Therefore, our findings highlight the critical role of cassava SR proteins as regulators of RNA splicing and salt tolerance in planta.

Identification and Regulation of Tomato Serine/Arginine-Rich Proteins Under High Temperatures

“…Indeed, with the exception of Sl-RSZ21a, all other SR and SR-like genes are alternatively spliced (Figure 4). The absence of alternative splicing in at least one RSZ gene has been reported in A. thaliana, B. rapa, and Manihot esculenta (cassava) (Palusa et al, 2007;Yoon et al, 2018;Gu et al, 2020). Moreover, the conservation in alternative splicing between Arabidopsis and rice SR genes, for example in the introns flanking the RRM coding region (Kalyna et al, 2006), is confirmed here for tomato (Figure 4).…”

“…The ortholog of NAC protein Solyc11g017470 in A. thaliana (AT1G01720) is induced after a treatment with abscisic acid (ABA) and is involved in abiotic stress responses (Jensen et al, 2013). An ABA-dependent regulation has been shown for several Arabidopsis and cassava SRs (Cruz et al, 2014;Gu et al, 2020) and therefore, considering that ABA is involved in HS response, we can assume an interplay of different regulatory networks to control SR transcription under high temperatures.…”

Plant RNA Binding Proteins as Critical Modulators in Drought, High Salinity, Heat, and Cold Stress Responses: An Updated Overview

“…Additionally, a few SR-like genes (e.g., SR45, SR45a) were found to have two RS domains instead of the one found in typical SR proteins [45,100,101]. Genome-wide identification of SR proteins in Brassica rapa [20], wheat, Brachypodium distachyon [44], tomato [36], and Cassava [43] resulted in 28, 40, 18, 19, and 18 SR genes, respectively. Of these, the expression of 22 and alternative splicing patterns of 17 genes in B. rapa were significantly altered in response to cold, heat, or oxidative stresses [20].…”

“…SR proteins are non-small nuclear ribonucleoproteins (non-snRNP) which form complex spliceosome machinery that mediates numerous events in pre-mRNA splicing [20,97]. The canonical SR domain proteins consist of one or two N-terminal RNA recognition motifs (RRMs), which bind to the RNA targets, and a serine-arginine or arginine-serine dipeptide-rich C-terminal-terminal region (RS domain) with a variable length [36,43,97]. Based on the domain organization structures and the presence of amino acid sequence motifs, SR proteins can be classified into six subfamilies: SR (two RRM), RS (two RRM, but the second RRM lacks SWQDLKD motif), SC (with just 1 RRM), SCL (SC-like with charged N terminal AA residues), RSZ (CCHC zinc knuckle), and RS2Z (two CCHC zinc knuckles) [44,98,99].…”

“…Heat stress (37.5 • C) enhanced the expression of six tomato SR genes (Sl-RS28, Sl-SR32, Sl-SR33, Sl-SC30b, Sl-RS2Z36, and Sl-SR46a) in leaves (Table 3). Overexpression of the cassava SR gene MeSR34 in Arabidopsis helped plants maintain reactive oxygen species homeostasis and increased the expression of osmotic stress-related genes, which eventually led to salt tolerance [43].…”