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Plant serine/arginine‐rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses

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Abstract Global analyses of splicing of precursor messenger RNAs (pre‐mRNAs) have revealed that alternative splicing (AS) is highly pervasive in plants. Despite the widespread occurrence of AS in plants, the mechanisms that control splicing and the roles of splice variants generated from a gene are poorly understood. Studies on plant serine/arginine‐rich (SR) proteins, a family of highly conserved proteins, suggest their role in both constitutive splicing and AS of pre‐mRNAs. SR proteins have a characteristic domain structure consisting of one or two RNA recognition motifs at the N‐terminus and a C‐terminal RS domain rich in arginine/serine dipeptides. Plants have many more SR proteins compared to animals including several plant‐specific subfamilies. Pre‐mRNAs of plant SR proteins are extensively alternatively spliced to increase the transcript complexity by about six‐fold. Some of this AS is controlled in a tissue‐ and development‐specific manner. Furthermore, AS of SR pre‐mRNAs is altered by various stresses, raising the possibility of rapid reprogramming of the whole transcriptome by external signals through regulation of the splicing of these master regulators of splicing. Most SR splice variants contain a premature termination codon and are degraded by up‐frameshift 3 (UPF3)‐mediated nonsense‐mediated decay (NMD), suggesting a link between NMD and regulation of expression of the functional transcripts of SR proteins. Limited functional studies with plant SRs suggest key roles in growth and development and plant responses to the environment. Here, we discuss the current status of research on plant SRs and some promising approaches to address many unanswered questions about plant SRs. WIREs RNA 2011 2 875–889 DOI: 10.1002/wrna.98 This article is categorized under: RNA Processing > Splicing Mechanisms RNA Processing > Splicing Regulation/Alternative Splicing

Schematic diagram showing different domains and their organization in different subfamilies of plant serine/arginine‐rich (SR) proteins. The Arabidopsis SR proteins in each subfamily and corresponding human orthologs are shown at the right of the schematic diagram. The old names of mammalian SRs are shown in parenthesis. In addition to the three mammalian SRs that are shown here, there are nine other SRs (SRSF3, 4, 5, 6, 9, 10, 11, and 12)18 that have no orthologs in flowering plants. RRM, RNA recognition motif. (Reprinted with permission from Ref 19. Copyright 2010 American Society of Plant Biologists)

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Bimolecular fluorescence complementation (BiFC)‐based mapping of SR45 domains involved in its association with U1‐70K. Different domains of SR45 that are fused to YFPc (middle) were introduced into protoplasts along with U1‐70K fused to YFPn (right) and visualized for reconstitution of yellow fluorescent protein (YFP) (right). RRM, RNA recognition motif; RS1 and RS2, arginine/serine‐rich domains 1 and 2. (Reprinted with permission from Ref 79. Copyright 2008 PLoS ONE)

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Effect of stresses on SR45 localization in root epidermal cells of GFP‐SR45 expressing Arabidopsis seedlings. Cold treatment relocalized GFP‐SR45 mostly to the nucleoplasmic pool, whereas heat treatment induced redistribution of GFP‐SR45 into irregularly shaped compartments. Controls were incubated at 22°C. (Reprinted with permission from Ref 91. Copyright 2003 Blackwell Publishing)

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Role of SR45 in flowering and alternative splicing. (a) sr45 mutant is late flowering. Left, wild type; right, sr45 mutant. (b) Expression and alternative splicing of precursor messenger RNA (pre‐mRNA) of one of the serine/arginine‐rich (SR) genes (SR30) in different organs in the mutant. An equal amount of template in each reaction was verified by amplifying a constitutively expressed cyclophilin (Cyc). DNA sizes are indicated on the right. Isoform number is indicated on the left side of the gel. I, inflorescence; L, leaf; R, root; S, stem. Schematic diagram in the bottom panel of SR30 shows the gene structure and its alternatively spliced messenger RNA (mRNA) isoforms. (Numbers below each isoform indicate the number of nucleotides.) Predicted proteins from splice variants are shown to the right of each isoform. Exons are filled rectangles and introns are thin lines. Black rectangles represent constitutively spliced exons, whereas the red rectangles indicate the included regions in splice variants. Vertical arrowhead and ‘*’ show start and stop codons, respectively. Horizontal green and red arrowheads above and below gene structures indicate the position of forward and reverse primers, respectively. In the schematics of predicted proteins, numbers to the right are the number of amino acids in the protein. RRM, RNA recognition motif; RS, arginine/serine‐rich domain. Blue rectangle indicates a stretch of amino acids that are not present in functional SR proteins. (Reprinted with permission from Ref 88. Copyright 2007 PLoS ONE)

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Roles of plant serine/arginine‐rich (SR) proteins in precursor messenger RNAs (pre‐mRNAs) splicing. SR proteins bind to sequences in exons, called exonic splicing regulators (ESRs), and then recruit and stabilize U1 small nuclear ribonucleoprotein (snRNP) on the 5′ splice site (5′ ss) and the heterodimeric U2AF complex to the 3′ splice site (3′ ss) and U2 snRNP to the adjacent branch point. They also mediate interaction between the U2AF complex and U1 snRNP across an exon or by binding to RNA sequences called intronic splicing regulators (ISRs) in introns to mediate interaction between the U2AF complex and U1 snRNP across introns.

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Analysis of expression and splicing of Arabidopsis serine/arginine‐rich (SR) genes in root, stem, leaf, inflorescence, and pollen. An equal amount of cDNA was used in polymerase chain reaction (PCR) with primers specific to each SR gene. An equal amount of template in each reaction was verified by amplifying a constitutively expressed cyclophilin. The name of the SR gene is shown on the left of each panel. Asterisks indicate the transcripts that encode full‐length proteins. Arrows indicate DNA sizes in bp. (Reprinted with permission from Ref 30. Copyright 2007 Blackwell Publishing)

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Effect of heat and cold on serine/arginine‐rich (SR) genes' expression and alternative splicing. Two‐week‐old seedlings were treated with cold at 4°C for 24 h and heat at 38°C for 6 h. RNA from control and treated samples was used for RT‐PCR. (Reprinted with permission from Ref 30. Copyright 2007 Blackwell Publishing)

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Splice variants generated from serine/arginine‐rich (SR) genes in Arabidopsis wild‐type and upf3 mutant plants. Forward and reverse primers corresponding to first and last exons, respectively, were used in RT‐PCR. The name of the gene is shown on the left of each gel. A constitutively expressed cyclophilin was used to verify an equal amount of template. Asterisks indicate the transcript(s) for each gene that encodes a full‐length protein. Splice variants with a premature termination codon (PTC) that are accumulated in the mutant are denoted with arrows. (Reprinted with permission from Ref 45. Copyright 2010 Blackwell Publishing)

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Schematic diagrams of alternatively spliced transcripts and predicted proteins from splice variants of Arabidopsis serine/arginine‐rich (SR) genes. Genes encoding SR subfamily (a), SC35 and SCL subfamilies (b), plant‐specific arginine/serine‐rich (RS) subfamily (c), and plant‐specific RS2Z family SRs (d). The name of the SR gene is shown on the left of each panel. The schematic diagram for each gene shows the gene structure and its splice variants. (Numbers below each isoform indicate the length of transcript in nucleotides.) Isoforms are numbered in ascending order according to the size (isoform 1 represents the smallest transcript). In all cases, except SR34b, SCL33, and SCL30a, the smallest transcript (isoform 1) encodes a full‐length protein. Predicted proteins from splice variants are shown to the right of each isoform. Exons are filled rectangles and introns are thin lines. Black rectangles represent constitutively spliced exons, whereas the red rectangles indicate the included regions in splice variants. Vertical arrowhead and ‘*’ show start and stop codons, respectively. Horizontal green and red arrowheads above and below gene structures indicate the position of forward and reverse primers, respectively. In the schematics of predicted proteins, numbers to the right are the number of amino acids in the protein. PSK, a domain rich in proline, serine, and lysine; RRM, RNA recognition motif. Blue rectangle indicates a stretch of amino acids that are not present in functional SR proteins. (Reprinted with permission from Ref 30. Copyright 2007 Blackwell Publishing)

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