At-RS31 orchestrates hierarchical cross-regulation of splicing factors and integrates alternative splicing with TOR-ABA pathways

Koster, T.; Venhuizen, P.; Lewinski, M.; Petrillo, E.; Marquez, Y.; Fuchs, A.; Ray, D.; Nimeth, B. A.; Riegler, S.; Franzmeier, S.; Zhong, H.; Hudges, T.; Morris, Q.; Barta, A.; Staiger, D.; Kalyna, M.

doi:10.1101/2024.12.04.626797

bioRxiv · 10.1101/2024.12.04.626797

At-RS31 orchestrates hierarchical cross-regulation of splicing factors and integrates alternative splicing with TOR-ABA pathways

Koster, T.·Venhuizen, P.·Lewinski, M.·Petrillo, E.·Marquez, Y.·Fuchs, A.·Ray, D.·Nimeth, B. A.·Riegler, S.·Franzmeier, S.·Zhong, H.·Hudges, T.·Morris, Q.·Barta, A.·Staiger, D.·Kalyna, M.

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Abstract

O_LIAlternative splicing is essential for plants, enabling a single gene to produce multiple transcript variants to boost functional diversity and fine-tune responses to environmental and developmental cues. At-RS31, a plant-specific splicing factor in the Serine/Arginine (SR)-rich protein family, responds to light and the Target of Rapamycin (TOR) signaling pathway, yet its downstream targets and regulatory impact remain unknown. C_LIO_LITo identify At-RS31 targets, we applied individual-nucleotide resolution crosslinking and immunoprecipitation (iCLIP) and RNAcompete assays. Transcriptomic analyses of At-RS31 mutant and overexpressing plants further revealed its effects on alternative splicing. C_LIO_LIiCLIP identified 4,034 At-RS31 binding sites across 1,421 genes, enriched in CU-rich and CAGA RNA motifs. Comparative iCLIP and RNAcompete data indicate that the RS domain of At-RS31 may influence its binding specificity in planta, underscoring the value of combining in vivo and in vitro approaches. Transcriptomic analysis showed that At-RS31 modulates diverse splicing events, particularly intron retention and exitron splicing, and influences other splicing modulators, acting as a hierarchical regulator. C_LIO_LIBy regulating stress-response genes and genes in both TOR and abscisic acid (ABA) signaling pathways, At-RS31 may help integrate these signals, balancing plant growth with environmental adaptability through alternative splicing. C_LI

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Koster, T., Venhuizen, P., Lewinski, M., Petrillo, E., Marquez, Y., Fuchs, A., Ray, D., Nimeth, B. A., Riegler, S., Franzmeier, S., Zhong, H., Hudges, T., Morris, Q., Barta, A., Staiger, D., Kalyna, M.. 2024-12-07. At-RS31 orchestrates hierarchical cross-regulation of splicing factors and integrates alternative splicing with TOR-ABA pathways. https://doi.org/10.1101/2024.12.04.626797

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