A fungal pathogen suppresses host leaf senescence to increase infection

Phytopathogens such as Puccinia striiformis f. sp. tritici (Pst) induce pigment retention at pathogen infection sites. Although pigment retention is commonly observed in diverse pathosystems, its underlying physiological mechanism remains largely unclear. Herein, we identify and characterize a wheat leaf senescence gene, TaSGR1, which enhances resistance against Pst by promoting leaf senescence and H2O2 accumulation while inhibiting photosynthesis. Knockout of TaSGR1 (STAYGREEN) in wheat increases pigment retention and plant susceptibility. Pst_TTP1 (TaTrx-Targeting Protein 1), a secreted rust fungal effector critical for Pst virulence, binds to the plastidial thioredoxin TaTrx (Thioredoxin), preventing its translocation into chloroplasts. Within the chloroplasts, TaTrx catalyzes the transformation of TaSGR1 oligomers into monomers. These TaSGR1 monomers accumulate in the chloroplasts, accelerating leaf senescence, H2O2 accumulation, and cell death. The inhibition of this oligomer-to-monomer transformation, caused by the failure of TaTrx to enter the chloroplast due to Pst_TTP1, impairs plant resistance against Pst. Overall, our study reveals the suppression of redox signaling cascade that catalyzes the transformation of TaSGR1 oligomers into monomers within chloroplasts and the inhibition of leaf chlorosis by rust effectors as key mechanisms underlying disease susceptibility. One effector of wheat disease pathogen is found to prevent the entry of thioredoxin into chloroplast. This disrupts the thioredoxin-mediated monomerization of STAYGREEN, a key regulator of senescence, and thereby suppresses plant defense responses.