Contrasting functions ofArabidopsisSUMO1/2 isoforms with SUMO3 intersect to modulate innate immunity and global SUMOylome responses
Authors: Dnyaneshwar Ingole Kishor , Kasera Mritunjay , van den Burg Harrold A. , Bhattacharjee Saikat 
Published: May 2020

Reversible covalent attachment of SMALL UBIQUITIN-LIKE MODIFIERS (SUMOs) on target proteins regulate diverse cellular process across all eukaryotes. InArabidopsis thaliana, most mutants with perturbed global SUMOylome display severe impairments in growth and adaptations to physiological stresses. Since SUMOs self-regulate activities of SUMOylation-associated proteins, existence of multiple isoforms introduces possibilities of their functional intersections which remain unexplored especially in plant systems. Using well-established defense responses elicited against virulent and avirulentPseudomonas syringaepv.tomatostrains, we investigated crosstalks in individual and combinatorial Arabidopsissummutants. Here we report that whileSUM1andSUM2additively, but not equivalently suppress basal and TNL-specific immunity via down-regulation of salicylic acid (SA)-dependent responses,SUM3promotes these defenses genetically downstream of SA. Remarkably, the expression ofSUM3is transcriptionally suppressed by SUMO1 or SUMO2. The loss ofSUM3not only lowers basal or post-bacterial challenge responsive enhancements of SUMO1/2-congugates but also reduces upregulation dynamics of defensive proteins and SUMOylation-associated transcripts. Combining asum3mutation partially attenuates heightened immunity ofsum1orsum2mutants suggesting intricate functional impingements among these isoforms in optimizing immune amplitudes. SimilarSUM1-SUM3intersections also affect global SUMOylome responses to heat-shock affecting most notably the induction of selective heat-shock transcription factors. Overall, our investigations reveal novel insights into auto-regulatory mechanisms among SUMO isoforms in host SUMOylome maintenance and adjustments to environmental challenges.

Author Summary

In plants, similar to animals, protein functions are regulated at multiple levels. One prevalent mode is to allow covalent linkage of small proteins to specific amino acids on targets thereby affecting its fate and function. One such kind of modification named as SUMOylation involves attachment of SUMO proteins. A plant maintains strict control over its pool of SUMOylated proteins (termed SUMOylome) which upon biotic or abiotic stresses are altered to facilitate appropriate responses, returning back to steady-state when the threat subsides. In mutants of the model plantArabidopsis thalianahaving disturbed steady-state SUMOylome, growth and developmental defects ensue. These mutants are auto-immune showing more resistance to infection by the bacterial pathogenPseudomonas syringae. However, Arabidopsis SUMO-family are comprised of multiple members raising the question about their specificity or functional crosstalks. We discovered that two SUMO members function in coordination to suppress immunity including the repression of a third member which supports defenses. The expression of this third member during pathogen attack or heat-shock influences the responsive changes in the host SUMOylome likely suggesting SUMOs themselves play vital role in these adaptations. Overall, our work highlights novel intersections of SUMO members in mounting stress-specific responses.