ACCELERATED CELL DEATH 6 (ACD6) mediates a trade-off between growth and defense in Arabidopsis thaliana. However, the precise biochemical mechanism by which ACD6 and related proteins in plants act remains enigmatic. Here, we identified two loci, MODULATOR OF HYPERACTIVE ACD6 1 (MHA1) and its paralog MHA1-LIKE (MHA1L), that code for ~7 kDa proteins that differentially interact with specific ACD6 variants. MHA1L enhances accumulation of an ACD6 complex, thereby increasing activity of the ACD6 standard allele for regulating plant growth and defenses. ACD6 is a multipass transmembrane protein with intracellular ankyrin repeats that are structurally similar to those found in mammalian ion channels. Several lines of evidence link increased ACD6 activity to enhanced calcium influx, likely mediated by ACD6 itself and with MHA1L as a direct regulator of ACD6.

Plants deploy intracellular receptors to counteract pathogen effectors that suppress cell-surface receptor-mediated immunity. To what extent pathogens manipulate also immunity mediated by intracellular receptors, and how plants tackle such manipulation, remains unknown. Arabidopsis thaliana encodes three very similar ADR1 class helper NLRs (ADR1, ADR1-L1 and ADR1-L2), which play key roles in plant immunity initiated by intracellular receptors. Here, we report that Pseudomonas syringae AvrPtoB, an effector with E3 ligase activity, can suppress ADR1-L1- and ADR1-L2-mediated cell death. ADR1, however, evades such suppression by diversification of two ubiquitination sites targeted by AvrPtoB. The intracellular sensor NLR SNC1 interacts with and guards the CCR domains of ADR1-L1 and ADR-L2. Removal of ADR1-L1 and ADR1-L2 or delivery of AvrPtoB activates SNC1, which then signals through ADR1 to trigger immunity. Our work not only uncovers the long sought-after physiological function of SNC1 in pathogen defense, but also that reveals how plants can use dual strategies, sequence diversification and a multiple layered guard-guardee system, to counteract pathogen attack on core immunity functions.

Maize is one of the most important crops for food, cattle feed and energy production. However, maize is frequently attacked by various pathogens and pests, which pose a significant threat to maize yield and quality. Identification of quantitative trait loci and genes for resistance to pests will provide the basis for resistance breeding in maize. Here, a β-glucosidase ZmBGLU17 was identified as a resistance gene against Pythium aphanidermatum, one of the causal agents of corn stalk rot, by genome-wide association analysis. Genetic analysis showed that both structural variations at the promoter and a single nucleotide polymorphism at the fifth intron distinguish the two ZmBGLU17 alleles. The causative polymorphism near the GT-AG splice site activates cryptic alternative splicing and intron retention of ZmBGLU17 mRNA, leading to the downregulation of functional ZmBGLU17 transcripts. ZmBGLU17 localizes in both the extracellular matrix and vacuole and contribute to the accumulation of two defense metabolites lignin and DIMBOA. Silencing of ZmBGLU17 reduces maize resistance against P. aphanidermatum, while overexpression significantly enhances resistance of maize against both the oomycete pathogen P. aphanidermatum and the Asian corn borer Ostrinia furnacalis. Notably, ZmBGLU17 overexpression lines exhibited normal growth and yield phenotype in the field. Taken together, our findings reveal that the apoplastic and vacuolar localized ZmBGLU17 confers resistance to both pathogens and insect pests in maize without a yield penalty, by fine-tuning the accumulation of lignin and DIMBOA.