TheHVE/CAND1gene is required for the early patterning of leaf venation inArabidopsis

Abstract

The hemivenata-1 (hve-1) recessive allele was isolated in a search for natural variations in the leaf venation pattern of Arabidopsis thaliana, where it was seen to cause extremely simple venation in vegetative leaves and cotyledons, increased shoot branching, and reduced root waving and fertility, traits that are reminiscent of some mutants deficient in auxin signaling. Reduced sensitivity to exogenous auxin was found in the hve-1 mutant, which otherwise displayed a wild-type response to auxin transport inhibitors. The HVE gene was positionally cloned and found to encode a CAND1 protein. The hve-1 mutation caused mis-splicing of the transcripts of the HVE/CAND1 gene and a vein phenotype indistinguishable from that of hve-2 and hve-3, two putatively null T-DNA alleles. Inflorescence size and fertility were more affected by hve-2 and hve-3, suggesting that hve-1 is hypomorphic. The simple venation pattern of hve plants seems to arise from an early patterning defect. We found that HVE/CAND1 binds to CULLIN1, and that the venation patterns of axr1 and hve mutants are similar, which suggest that ubiquitin-mediated auxin signaling is required for venation patterning in laminar organs, the only exception being cauline leaves. Our analyses of double mutant and transgenic plants indicated that auxin transport and perception act independently to pattern leaf veins, and that the HVE/CAND1 gene acts upstream of ATHB-8 at least in higher order veins, in a pathway that involves AXR1, but not LOP1, PIN1, CVP1 or CVP2.

Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves

“…Furthermore, initially-wide fields of DOF expression became laterally confined over time, while ATHB8 expression domains are always narrow at inception and progress longitudinally during vein formation. In this respect, expression of DOF2.1, DOF4.6 and DOF5.3 resembles that of genes that have been functionally implicated in selection of ATHB8-expressing preprocambial cells [e.g., (Alonso-Peral et al, 2006;Carland and Nelson, 2004;Donner et al, 2009;Hardtke and Berleth, 1998;Petricka and Nelson, 2007;Sawa et al, 2005;Sawchuk et al, 2007;Scarpella et al, 2006)]. However, DOF2.1, DOF4.6 and DOF5.3 are not expected to be directly involved in this process because preprocambial expression of ATHB8 is under the immediate control of MP through a noncanonical auxin response element located in the ATHB8 promoter (Donner et al, 2009).…”

“…Initiation of ATHB8 expression is directly controlled by MP (Donner et al, 2009), and identifies acquisition of a critical and typically irreversible 'preprocambial' cell state that accurately predicts sites of vascular differentiation (Alonso-Peral et al, 2006;Candela et al, 2001;Carland and Nelson, 2004;Cnops et al, 2006;Donner et al, 2009;Kang and Dengler, 2004;Koizumi et al, 2000;Petricka and Nelson, 2007;Pineau et al, 2005;Sawchuk et al, 2007Sawchuk et al, , 2008Scarpella et al, 2004Scarpella et al, , 2006. A view of the transcriptional landscape of cells at preprocambial stages would be particularly valuable as it might provide insight into the molecular pathways underlying vein formation.…”

“…A view of the transcriptional landscape of cells at preprocambial stages would be particularly valuable as it might provide insight into the molecular pathways underlying vein formation. However, very few genes have been identified whose expression is initiated at stages prior to procambium formation [e.g., (Alonso-Peral et al, 2006;Baima et al, 1995;Carland and Nelson, 2009;Hardtke and Berleth, 1998;Kang and Dengler, 2004;Konishi and Yanagisawa, 2007;Scarpella et al, 2004;Steinmann et al, 1999;Wenzel et al, 2007)].…”

Isolation and Characterization ofcul1-7, a Recessive Allele ofCULLIN1That Disrupts SCF Function at the C Terminus of CUL1 inArabidopsis thaliana

“…In many cases, slowed degradation of the mutant protein was experimentally verified (Timpte et al 1994;Leyser et al 1996;Rouse et al 1998;Nagpal et al 2000;Tian et al 2002;Tatematsu et al 2004;Yang et al 2004). Other auxin response mutants include plants with defective subunits of the SCF ubiquitin E3 ligase or mutations that cause misregulation of SCF activity/ assembly (Ruegger et al 1998;Gray et al 2003;Hellmann et al 2003;Cheng et al 2004;Chuang et al 2004;Feng et al 2004;Dharmasiri et al 2005b;Quint et al 2005;Alonso-Peral et al 2006;Walsh et al 2006;Moon et al 2007;Woodward et al 2007).…”

Lessons from a search for leaf mutants in Arabidopsis thaliana

“…hve-1 reduces the complexity of the venation pattern in leaves and cotyledons. The HVE1 gene encodes the Arabidopsis thaliana ortholog of the mammalian CAND1 protein (Alonso-Peral et al, 2006), which binds to unneddylated CULLIN1 (CUL1), a protein that forms part of the SCF ubiquitin ligase complexes that regulate target protein degradation through the 26S proteasome. Similar venation patterns in auxin resistant1 (axr1), a mutant insensitive to auxin, and hve mutants indicate that auxin signaling mediated by ubiquitination is required for venation patterning in Arabidopsis thaliana leaves (Alonso-Peral et al, 2006).…”