Genome-scale analysis of Arabidopsis splicing-related protein kinase families reveals roles in abiotic stress adaptation
Abstract Nearly 60 – 80 % of intron-containing plant genes undergo alternative splicing in response to either stress or plant developmental cues. RNA splicing is performed by a large ribonucleoprotein complex called the spliceosome in conjunction with associated subunits such as serine arginine (SR)...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-10-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-022-03870-9 |
| _version_ | 1797818071697588224 |
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| author | M. C. Rodriguez Gallo Q. Li D. Mehta R. G. Uhrig |
| author_facet | M. C. Rodriguez Gallo Q. Li D. Mehta R. G. Uhrig |
| author_sort | M. C. Rodriguez Gallo |
| collection | DOAJ |
| description | Abstract Nearly 60 – 80 % of intron-containing plant genes undergo alternative splicing in response to either stress or plant developmental cues. RNA splicing is performed by a large ribonucleoprotein complex called the spliceosome in conjunction with associated subunits such as serine arginine (SR) proteins, all of which undergo extensive phosphorylation. In plants, there are three main protein kinase families suggested to phosphorylate core spliceosome subunits and related splicing factors based on orthology to human splicing-related kinases: the SERINE/ARGININE PROTEIN KINASES (SRPK), ARABIDOPSIS FUS3 COMPLEMENT (AFC), and Pre-mRNA PROCESSING FACTOR 4 (PRP4K) protein kinases. To better define the conservation and role(s) of these kinases in plants, we performed a genome-scale analysis of the three families across photosynthetic eukaryotes, followed by extensive transcriptomic and bioinformatic analysis of all Arabidopsis thaliana SRPK, AFC, and PRP4K protein kinases to elucidate their biological functions. Unexpectedly, this revealed the existence of SRPK and AFC phylogenetic groups with distinct promoter elements and patterns of transcriptional response to abiotic stress, while PRP4Ks possess no phylogenetic sub-divisions, suggestive of functional redundancy. We also reveal splicing-related kinase families are both diel and photoperiod regulated, implicating different orthologs as discrete time-of-day RNA splicing regulators. This foundational work establishes a number of new hypotheses regarding how reversible spliceosome phosphorylation contributes to both diel plant cell regulation and abiotic stress adaptation in plants. |
| first_indexed | 2024-03-13T09:03:43Z |
| format | Article |
| id | doaj.art-7d45d2377e7b425293e56153ae312c6d |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-03-13T09:03:43Z |
| publishDate | 2022-10-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-7d45d2377e7b425293e56153ae312c6d2023-05-28T11:12:25ZengBMCBMC Plant Biology1471-22292022-10-0122112210.1186/s12870-022-03870-9Genome-scale analysis of Arabidopsis splicing-related protein kinase families reveals roles in abiotic stress adaptationM. C. Rodriguez Gallo0Q. Li1D. Mehta2R. G. Uhrig3Department of Biological Sciences, University of AlbertaDepartment of Biological Sciences, University of AlbertaDepartment of Biological Sciences, University of AlbertaDepartment of Biological Sciences, University of AlbertaAbstract Nearly 60 – 80 % of intron-containing plant genes undergo alternative splicing in response to either stress or plant developmental cues. RNA splicing is performed by a large ribonucleoprotein complex called the spliceosome in conjunction with associated subunits such as serine arginine (SR) proteins, all of which undergo extensive phosphorylation. In plants, there are three main protein kinase families suggested to phosphorylate core spliceosome subunits and related splicing factors based on orthology to human splicing-related kinases: the SERINE/ARGININE PROTEIN KINASES (SRPK), ARABIDOPSIS FUS3 COMPLEMENT (AFC), and Pre-mRNA PROCESSING FACTOR 4 (PRP4K) protein kinases. To better define the conservation and role(s) of these kinases in plants, we performed a genome-scale analysis of the three families across photosynthetic eukaryotes, followed by extensive transcriptomic and bioinformatic analysis of all Arabidopsis thaliana SRPK, AFC, and PRP4K protein kinases to elucidate their biological functions. Unexpectedly, this revealed the existence of SRPK and AFC phylogenetic groups with distinct promoter elements and patterns of transcriptional response to abiotic stress, while PRP4Ks possess no phylogenetic sub-divisions, suggestive of functional redundancy. We also reveal splicing-related kinase families are both diel and photoperiod regulated, implicating different orthologs as discrete time-of-day RNA splicing regulators. This foundational work establishes a number of new hypotheses regarding how reversible spliceosome phosphorylation contributes to both diel plant cell regulation and abiotic stress adaptation in plants.https://doi.org/10.1186/s12870-022-03870-9Abiotic StressEvolutionDiel cyclemRNA splicingProtein kinases |
| spellingShingle | M. C. Rodriguez Gallo Q. Li D. Mehta R. G. Uhrig Genome-scale analysis of Arabidopsis splicing-related protein kinase families reveals roles in abiotic stress adaptation BMC Plant Biology Abiotic Stress Evolution Diel cycle mRNA splicing Protein kinases |
| title | Genome-scale analysis of Arabidopsis splicing-related protein kinase families reveals roles in abiotic stress adaptation |
| title_full | Genome-scale analysis of Arabidopsis splicing-related protein kinase families reveals roles in abiotic stress adaptation |
| title_fullStr | Genome-scale analysis of Arabidopsis splicing-related protein kinase families reveals roles in abiotic stress adaptation |
| title_full_unstemmed | Genome-scale analysis of Arabidopsis splicing-related protein kinase families reveals roles in abiotic stress adaptation |
| title_short | Genome-scale analysis of Arabidopsis splicing-related protein kinase families reveals roles in abiotic stress adaptation |
| title_sort | genome scale analysis of arabidopsis splicing related protein kinase families reveals roles in abiotic stress adaptation |
| topic | Abiotic Stress Evolution Diel cycle mRNA splicing Protein kinases |
| url | https://doi.org/10.1186/s12870-022-03870-9 |
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