The RLCK-VND6 module coordinates secondary cell wall formation and adaptive growth in rice.

The orderly deposition of secondary cell wall (SCW) in plants is implicated in various biological programs and is precisely controlled. Although many positive and negative regulators have been documented, fine-tuning regulators of SCW formation that orchestrate distinct cellular physiologies have rarely been reported. Here, we report a SCW regulator Cellulose Synthase coexpressed Kinase1 (CSK1) and its signaling cascade in rice. Transcriptome deep sequencing of developing internodes and genome-wide co-expression assays revealed that a receptor-like cytoplasmic kinase CSK1 is co-expressed with cellulose synthase genes and is responsive to various stress stimuli. Increased SCW thickness and vigorous vessel transport of csk1 defines CSK1 as a negative regulator of SCW biosynthesis. Through observation of the signal of green fluorescent protein tagged CSK1 in rice protoplasts and stable transgenic plants, we found that CSK1 is localized in the nucleus and adjacent to the plasma membrane. Multiple lines of evidence demonstrated that CSK1 phosphorylates VASCULAR-RELATED NAC-DOMAIN 6 (VND6), a master SCW-associated transcription factor, in the nucleus, which alleviates the transcription of a suite of SCW-related genes, thereby attenuating SCW accumulation. Genetic studies validated that CSK1 functions upstream of VND6. Furthermore, physiological analyses revealed that CSK1 and VND6 implicate in abscisic acid-mediated stress signaling, which regulates cell growth and SCW deposition. The CSK1-VND6 module is necessary for the operation of SCW biosynthesis machinery, which coordinates SCW accumulation and growth plasticity. This study thus identifies a SCW fine-tuning regulator and outlines a mechanism for precise control of SCW deposition, offering tools for rationally tailoring agronomic traits.