TheRON1/FRY1/SAL1Gene Is Required for Leaf Morphogenesis and Venation Patterning in Arabidopsis

Abstract

To identify genes involved in vascular patterning in Arabidopsis (Arabidopsis thaliana), we screened for abnormal venation patterns in a large collection of leaf shape mutants isolated in our laboratory. The rotunda1-1 (ron1-1) mutant, initially isolated because of its rounded leaves, exhibited an open venation pattern, which resulted from an increased number of free-ending veins. We positionally cloned the RON1 gene and found it to be identical to FRY1/SAL1, which encodes an enzyme with inositol polyphosphate 1-phosphatase and 3#(2#),5#-bisphosphate nucleotidase activities and has not, to our knowledge, previously been related to venation patterning. The ron1-1 mutant and mutants affected in auxin homeostasis share perturbations in venation patterning, lateral root formation, root hair length, shoot branching, and apical dominance. These similarities prompted us to monitor the auxin response using a DR5-GUS auxin-responsive reporter transgene, the expression levels of which were increased in roots and reduced in leaves in the ron1-1 background. To gain insight into the function of RON1/FRY1/SAL1 during vascular development, we generated double mutants for genes involved in vein patterning and found that ron1 synergistically interacts with auxin resistant1 and hemivenata-1 but not with cotyledon vascular pattern1 (cvp1) and cvp2. These results suggest a role for inositol metabolism in the regulation of auxin responses. Microarray analysis of gene expression revealed that several hundred genes are misexpressed in ron1-1, which may explain the pleiotropic phenotype of this mutant. Metabolomic profiling of the ron1-1 mutant revealed changes in the levels of 38 metabolites, including myoinositol and indole-3-acetonitrile, a precursor of auxin.

ROTUNDA3 function in plant development by phosphatase 2A-mediated regulation of auxin transporter recycling

“…Hence, we hypothesized that the auxin-related phenotypes of ron3 are the consequence of altered PIN phosphorylation status and activity. Additional support came from the resemblance of the ron3 phenotypes to those of ron1, for which defective PIN polarity had been shown (14). The additive phenotypes in the double-mutant ron1 ron3 indicated that RON3 acts in a mode similar to that of RON1, corroborating a role for RON3 in PIN polarity-related processes.…”

“…The A. thaliana (L.) Heynh. lines are Ler and Col accessions (Nottingham Arabidopsis Seed Collection), ron3-1 and ron1-1 mutants (both Ler) (14), ron3-2 allele (GK374F12 line, homozygous for the T-DNA insertion in At4g24500; Col), rcn1 mutant (WS) (10), 35S::PID, and line PID21 (Col) (20,21). Media and growth conditions are discussed in SI Materials and Methods.…”

“…The ron3-1 (Ler) auxin-related phenotypes resemble those of the ron1-1 mutant (Ler) (14). The RON1 gene codes for an inositol polyphosphate 1-phosphatase that has a function in inositol triphosphate-mediated Ca 2+ signaling that also affects auxin transport and PIN polarity (15).…”

Genetic interaction of two abscisic acid signaling regulators, HY5 and FIERY1, in mediating lateral root formation

“…10,[17][18][19][20] Previously, we reported that HY5, a well-characterized component in the light signal transduction pathway, also mediates ABA response during seed germination and lateral root development. 21,22 Using the enhanced light response as a phenotype, we conducted a genetic screen and isolated fry1 suppressors with reduced light sensitivity.…”

Leaf Development

“…Phytohormone-dependent controls are not included in this review; readers interested in those controls may wish to consult the latest reviews on the roles for each phytohormone in the Arabidopsis Book. Understanding of genetic controls in tissue-or cell-type differentiations such as in leaf venation patterning has also advanced in recent years (e.g., Dengler and Kang 2001;Alonso-Peral et al 2006;Robles et al 2010), but these topics will be covered in another review article.…”