A CsNF-YB4-CsWAT1-CsARF9 regulatory cascade mediates auxin-dependent suppression of lignin biosynthesis and resistance to Colletotrichum camelliae in tea plants

Abstract

Tea plant (Camellia sinensis) is an economically important crop whose yield and quality are threatened by anthracnose caused by Colletotrichum camelliae. While C. camelliae infection elevates indole-3-acetic acid (IAA) levels in tea plants, how this hormone increases influences disease progression remains unclear. Here, we show that C. camelliae actively rewires auxin homeostasis in tea plants to compromise immunity. Using functional genomics and molecular analyses, we identified an auxin transporter, CsWAT1-19, which is associated with intracellular auxin compartmentalization. Its pathogen-induced expression is essential for cytosolic free IAA accumulation and subsequent disease development. We further delineated a regulatory cascade in which pathogen infection downregulates the transcriptional repressor CsNF-YB4, thereby relieving its repression of CsWAT1-19. The resulting increase in cytosolic free IAA activates the auxin-responsive factor CsARF9, which directly suppresses key lignin biosynthetic genes and disrupts cell wall-based defense. Together, our findings define a CsNF-YB4→CsWAT1-19→CsARF9 regulatory module through which a fungal pathogen hijacks host auxin transport and signaling to attenuate lignin-mediated physical barriers, providing new insight into the intersection of plant hormone signaling and immune responses in tea plants.