The Photoperiodic Flowering Time Regulator FKF1 Negatively Regulates Cellulose Biosynthesis

Abstract

Cellulose synthesis is precisely regulated by internal and external cues, and emerging evidence suggests that light regulates cellulose biosynthesis through specific light receptors. Recently, the blue light receptor CRYPTOCHROME 1 (CRY1) was shown to positively regulate secondary cell wall biosynthesis in Arabidopsis (<i>Arabidopsis thaliana</i>). Here, we characterize the role of <i>FLAVIN-BINDING KELCH REPEAT</i>, <i>F-BOX 1</i> (<i>FKF1</i>), another blue light receptor and well-known photoperiodic flowering time regulator, in cellulose biosynthesis. A phenotype suppression screen using a cellulose deficient mutant <i>cesa1^aegeus,cesa3^ixr1-2</i> (<i>c1,c3</i>), which carries nonlethal point mutations in <i>CELLULOSE SYNTHASE A 1</i> (<i>CESA1</i>) and <i>CESA3</i>, resulted in identification of the phenotype-restoring <i>large leaf</i> (<i>llf</i>) mutant. Next-generation mapping using the whole genome resequencing method identified the <i>llf</i> locus as <i>FKF1</i> <i>FKF1</i> was confirmed as the causal gene through observation of the <i>llf</i> phenotype in an independent triple mutant <i>c1,c3,fkf1-t</i> carrying a <i>FKF1</i> T-DNA insertion mutant. Moreover, overexpression of <i>FKF1</i> in <i>llf</i> plants restored the <i>c1,c3</i> phenotype. The <i>fkf1</i> mutants showed significant increases in cellulose content and <i>CESA</i> gene expression compared with that in wild-type Columbia-0 plants, suggesting a negative role of FKF1 in cellulose biosynthesis. Using genetic, molecular, and phenocopy and biochemical evidence, we have firmly established the role of FKF1 in regulation of cellulose biosynthesis. In addition, <i>CESA</i> expression analysis showed that diurnal expression patterns of <i>CESA</i>s are FKF1 independent, whereas their circadian expression patterns are FKF1 dependent. Overall, our work establishes a role of FKF1 in the regulation of cell wall biosynthesis in Arabidopsis.