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Steady-state SUMOylome of a plant is adjusted locally during developmental transitions and more globally during stress exposures. We recently reported that basal immunity in  Arabidopsis thaliana  against  Pseudomonas syringae  pv  tomato  strain DC3000 ( PstDC3000 ) is associated with strong enhancements in the net SUMOylome. Transcriptional upregulations of SUMO conjugases, suppression of protease, and increased SUMO translations accounted for this enhanced SUMOylation. Antagonistic roles of SUMO1/2 and SUMO3 isoforms further fine-tuned the SUMOylome adjustments, thus impacting defense amplitudes and immune outcomes. Loss of function of  SUPPRESSOR OF rps4-RLD1  ( SRFR1 ), a previously reported negative regulator of basal defenses, also caused constitutive increments in global SUMO-conjugates through similar modes. These suggest that SRFR1 plays a pivotal role in maintenance of SUMOylation homeostasis and its dynamic changes during immune elicitations. Here, we demonstrate that SRFR1 degradation kinetically precedes and likely provides the salicylic acid (SA) elevations necessary for the SUMOylome increments in basal defenses. We show that SRFR1 not only is a SUMOylation substrate but also interacts  in planta  with both SUMO1 and SUMO3. In  sum1  or  sum3  mutants, SRFR1 stabilities are reduced albeit by different modes. Whereas a  srfr1 sum1  combination is lethal, the  srfr1 sum3  plants retain developmental defects and enhanced immunity of the  srfr1  parent. Together with increasing evidence of SUMOs self-regulating biochemical efficiencies of SUMOylation-machinery, we present their impositions on SRFR1 expression that in turn counter-modulates the SUMOylome. Overall, our investigations reveal multifaceted dynamics of regulated SUMOylome changes via SRFR1 in defense-developmental balance.

frontiers in cell and developmental biology

Global SUMOylome Adjustments in Basal Defenses of Arabidopsis thaliana Involve Complex Interplay Between SMALL-UBIQUITIN LIKE MODIFIERs and the Negative Immune Regulator SUPPRESSOR OF rps4-RLD1