The protein modifier SUMO is critical for integrity of the Arabidopsis shoot apex at warm ambient temperatures

Abstract

SUMO is a protein modification whose conjugate levels peak during acute heat stress. We find that SUMO is also critical for plant longevity when Arabidopsis experiences a prolonged non-damaging period of only 28 degrees Celsius. Remarkably, this thermo-lethality at 28 degrees was not seen with any other mutant of the SUMO pathway tested. Autoimmunity due to low SUMO1/2 expression levels was not causal for this thermo-lethality. The role of SUMO for thermo-resilience was also distinct from its requirement for thermomorphogenesis – a growth response triggered by the same warm temperature, as only the latter response was dependent on the SUMO ligase SIZ1 as well. Thermo-resilience at 28 degrees Celsius and (acquired) thermotolerance (a response that allows plants to recover and acclimate to brief extreme temperatures) both depend on the HEAT SHOCK TRANSCRIPTION FACTOR A1 (HSFA1). Acquired thermotolerance was, however, normal in the sumo1/2 knockdown mutant. Thus, SUMO-dependent thermo-resilience is potentially controlled in a different way than the protein damage pathway that underpins thermotolerance. Close inspection of shoot apices revealed that the cell patterning and tissue integrity of the shoot apex of the SUMO1/2 knockdown mutant was lost at 28, but not 22 degrees Celsius. We thus describe a novel SUMO-dependent phenotype.

Post-translational modification: a strategic response to high temperature in plants

“…SUMOylation acts in a novel role, mediating the transcription switch mechanism between development and HS in plant cells by targeting different proteins (Han et al 2021). The interconnected dual role for SIZ1 and SUMO1/2 conjugation in the switch between plant immunity and high temperature-induced growth also supports this view (Hammoudi et al 2018(Hammoudi et al , 2021. In general, SUMOylation is vital for survival in stressful situations because it enables a swift reaction to a changing environment.…”

“…Van den Burg et al found that SUMO-dependent thermo-resilience can be potentially controlled in a different manner. SUMO1/2 activates temperature acclimation via the master regulator of heat stress: the HSFA1 family (Hammoudi et al 2021 ). This finding explained that SUMO1/2 have key roles in enabling plants to withstand prolonged warm periods.…”

Post-Translational Modifications in Histones and Their Role in Abiotic Stress Tolerance in Plants

“…Newer investigations have revealed that SUMO1/2 activation contributes to temperature acclimation through the HSFA1 family, recognized as the principal orchestrator of heat stress responses. Notably, mutant lines lacking SUMO1/2 exhibit thermosensitivity at 28 • C [169]. In a recent discovery by Zhang et al [168], an additional E3 ligase, the XB3 ortholog in Arabidopsis thaliana (XBAT31), has been identified.…”

OUP accepted manuscript

“…Another post-translational modification that is important in temperature signalling is SUMOylation. While SUMOylation is required for thermomorphogenesis and thermotolerance, SUMO-dependent thermoresilience is potentially controlled in a different way compared with the protein damage pathway that underpins thermotolerance (Hammoudi et al, 2021).…”