SUMOylation Inhibition Mediated by Disruption of SUMO E1-E2 Interactions Confers Plant Susceptibility to Necrotrophic Fungal Pathogens.
Protein modification by SUMO modulates essential biological processes in eukaryotes. SUMOylation is facilitated by sequential action of the E1-activating, E2-conjugating, and E3-ligase enzymes. In plants, SUMO regulates plant development and stress responses, which are key determinants in agricultural productivity. To generate additional tools for advancing our knowledge about the SUMO biology, we have developed a strategy for inhibiting in vivo SUMO conjugation based on disruption of SUMO E1-E2 interactions through expression of E1 SAE2UFDCtdomain. Targeted mutagenesis and phylogenetic analyses revealed that this inhibition involves a short motif in SAE2UFDCthighly divergent across kingdoms. Transgenic plants expressing the SAE2UFDCtdomain displayed dose-dependent inhibition of SUMO conjugation, and have revealed the existence of a post-transcriptional mechanism that regulates SUMO E2 conjugating enzyme levels. Interestingly, these transgenic plants displayed increased susceptibility to necrotrophic fungal infections by Botrytis cinerea and Plectosphaerella cucumerina. Early after fungal inoculation, host SUMO conjugation was post-transcriptionally downregulated, suggesting that targeting SUMOylation machinery could constitute a novel mechanism for fungal pathogenicity. These findings support the role of SUMOylation as a mechanism involved in plant protection from environmental stresses. In addition, the strategy for inhibiting SUMO conjugation in vivo described in this study might be applicable in important crop plants and other non-plant organisms regardless of their genetic complexity.
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Laura
L
Castaño-Miquel
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Abraham
A
Mas
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Inês
I
Teixeira
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Josep
J
Seguí
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Anna
A
Perearnau
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Bhagyasree N
BN
Thampi
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Arnaldo L
AL
Schapire
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Natalia
N
Rodrigo
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Gaelle
G
La Verde
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Silvia
S
Manrique
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain.
Maria
M
Coca
Center for Research in Agricultural Genomics - CRAG, Edifici CRAG-Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain. Electronic address: maria.lois@cragenomica.es.
L Maria
LM
Lois
D017360:Arabidopsis / Q000276:immunology / Q000378:metabolism / Q000382:microbiology*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D001203:Ascomycota / Q000502:physiology; D020171:Botrytis / Q000502:physiology; D018506:Gene Expression Regulation, Plant; D016296:Mutagenesis; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology*; D030821:Plants, Genetically Modified; D000072417:Protein Domains; D025841:Small Ubiquitin-Related Modifier Proteins / Q000037:antagonists & inhibitors / Q000378:metabolism*; D043743:Ubiquitin-Protein Ligase Complexes / Q000378:metabolism
D029681:Arabidopsis Proteins; D025841:Small Ubiquitin-Related Modifier Proteins; D043743:Ubiquitin-Protein Ligase Complexes
E1-activating enzyme; E1–E2 interaction disruption; SUMO inhibition; development; flowering; necrotrophic fungi