Fifty shades of SUMO: its role in immunity and at the fulcrum of the growth–defence balance

Abstract

The sessile nature of plants requires them to cope with an ever-changing environment. Effective adaptive responses require sophisticated cellular mechanisms at the post-transcriptional and post-translational levels. Post-translational modification by small ubiquitin-like modifier (SUMO) proteins is emerging as a key player in these adaptive responses. SUMO conjugation can rapidly change the overall fate of target proteins by altering their stability or interaction with partner proteins or DNA. SUMOylation entails an enzyme cascade that leads to the activation, conjugation and ligation of SUMO to lysine residues of target proteins. In addition to their SUMO processing activities, SUMO proteases also possess de-conjugative activity capable of cleaving SUMO from target proteins, providing reversibility and buffering to the pathway. These proteases play critical roles in the maintenance of the SUMO machinery in equilibrium. We hypothesize that SUMO proteases provide the all-important substrate specificity within the SUMO system. Furthermore, we provide an overview of the role of SUMO in plant innate immunity. SUMOylation also overlaps with multiple growth-promoting and defence-related hormone signalling pathways, and hence is pivotal for the maintenance of the growth-defence balance. This review aims to highlight the intricate molecular mechanisms utilized by SUMO to regulate plant defence and to stabilize the growth-defence equilibrium.

Regulation and Evolution of NLR Genes: A Close Interconnection for Plant Immunity

“…On the other hand, overexpression of the F-box protein CPR1 inhibits the growth defects and disease resistance of the siz1 mutant [ 136 ]. As SIZ1 and SUMO1/2 both act as important positive regulators of growth, the functional relationships between the different post-translational modifications on SNC1 might be responsible for the trade-off between thermo-morphogenesis and immune responses [ 138 ].…”

Specific TCP transcription factors interact with and stabilize PRR2 within different nuclear sub-domains

“…The identified SUMO attachment sites in PRR2 protein sequence are localized at positions 183 (LKQD) and 240 (VKEE) [54] that correspond to the same region previously described to be enriched in putative ubiquitination sites ( Figure 4A). The covalent conjugation of SUMO protein to its substrates regulates numerous cellular processes, including protein stability and activity in plants as well as in all eukaryotes [53,55,56]. Therefore, we cannot exclude that the results obtained Figure 4B could be explained with PRR2 SUMOylation, leading to a better-stabilized protein and/or any other modification in PRR2 protein properties including interacting activities.…”

Proteomic analysis of SUMO1-SUMOylome changes during defense elicitation inArabidopsis

“…Several studies have documented the importance of SUMO-modified proteins for basic growth, development and stress adaptations in eukaryotes (Castaño-miquel and Lois, 2016; de Vega et al 2018; Geiss-Friedlander and Melchior, 2007;Gill, 2004;Srivastava et al 2016;Verma et al 2018). In plant systems, barring few reports these remain largely understudied and the identity of differentially SUMOylated candidates connected to immune responses are very few (Colignon et al 2017a(Colignon et al , 2017bMazur et al 2017;Niu et al 2019;Saleh et al 2015).…”

“…From these reports, it is increasingly evident that unregulated increases (eds4-1, ots1/2 or over-expressing SUM1/2) or decreases (in siz1-2 or sum1-1 amiR-SUM2) in global SUMOylome bear immune consequences. It is also not surprising that pathogens attempt to manipulate host SUMOylome to increase their colonization efficiencies (Wimmer & Schreiner, 2015;Verma et al 2018). Several bacterial phytopathogenic effectors interfere with host SUMOylation as a mode to suppress immunity (Hotson et al 2003).…”