The Arabidopsis glutamate receptor-like gene GLR3.6 controls root development by repressing the Kip-related protein gene KRP4

In Arabidopsis, 20 genes encode putative glutamate receptor-like proteins (AtGLRs). However, the functions of most genes are unknown. In this study, our results revealed that loss of function of AtGLR3.6 (atglr3.6-1) leads to reduced primary root growth and fewer lateral roots, whereas AtGLR3.6 overexpression induced both primary and lateral root growth. The glr3.6-1 mutant exhibited a smaller root meristem size compared with the wild type, indicating that AtGLR3.6 controls root meristem size. In addition, atglr3.6-1 roots show a decreased mitotic activity accounting for the reduced root meristem size. Furthermore, expression of a gene encoding a cell cycle inhibitor, the cyclin-dependent kinase (CDK) inhibitor Kip-related protein 4 (KRP4), was significantly up-regulated in the mutant and down-regulated in AtGLR3.6-overexpressing roots, suggesting a role for KRP4 in AtGLR3.6-mediated root meristem maintenance. Importantly, the atglr3.6-1 mutant recovered most of its root growth when KRP4 expression is down-regulated, whereas elevated KRP4 expression in AtGLR3.6-overexpressing plants phenocopied the wild-type root growth, implying an underlying relationship between AtGLR3.6 and KRP4 genes. Cytosolic Ca2+ elevation is reduced in atglr3.6-1 roots, suggesting impaired calcium signaling. Moreover, calcium treatment reduced the level of KRP4 and hence induced root growth. Collectively, we reveal that AtGLR3.6 is required for primary and lateral root development, and KRP4 functions as a downstream signaling element in Arabidopsis thaliana.