Rice copine genes OsBON1 and OsBON3 function as suppressors of broad-spectrum disease resistance.

Breeding for disease resistance is the most effective strategy to control diseases, particularly with broad-spectrum disease resistance in many crops. However, knowledge on genes and mechanism of broad-spectrum resistance and trade-off between defence and growth in crops is limited. Here, we show that the rice copine genes OsBON1 and OsBON3 are critical suppressors of immunity. Both OsBON1 and OsBON3 changed their protein subcellular localization upon pathogen challenge. Knockdown of OsBON1 and dominant negative mutant of OsBON3 each enhanced resistance to rice bacterial and fungal pathogens with either hemibiotrophic or necrotrophic lifestyles. The defence activation in OsBON1 knockdown mutants was associated with reduced growth, both of which were largely suppressed under high temperature. In contrast, overexpression of OsBON1 or OsBON3 decreased disease resistance and promoted plant growth. However, neither OsBON1 nor OsBON3 could rescue the dwarf phenotype of the Arabidopsis BON1 knockout mutant, suggesting a divergence of the rice and Arabidopsis copine genes. Our study therefore shows that the rice copine genes play a negative role in regulating disease resistance and their expression level and protein location likely have a large impact on the balance between immunity and agronomic traits.

Identification and analysis of copine/BONZAI proteins among evolutionarily diverse plant species.

Copines are evolutionarily conserved calcium-dependent membrane-binding proteins with potentially critical biological functions. In plants, the function of these proteins has not been analyzed except for in Arabidopsis thaliana where they play critical roles in development and disease resistance. To facilitate functional studies of copine proteins in crop plants, genome-wide identification, curation, and phylogeny analysis of copines in 16 selected plant species were conducted. All the identified 32 plant copines have conserved features of the two C2 domains (C2A and C2B) and the von Willebrand factor A (vWA) domain. Different from animal and protozoa copines, plant copines have glycine at the second residue potentially acquiring a unique protein myristoylation modification. Phylogenetic analysis suggests that copine was present as one copy when evolving from green algae to basal flowering plants, and duplicated before the divergence of monocots and dicots. In addition, gene expression and protein localization study of rice copines suggests both conserved and different properties of copines in dicots and monocots. This study will contribute to uncovering the role of copine genes in different plant species.