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Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms.

Thomann A, Lechner E, Hansen M, Dumbliauskas E, Parmentier Y, Kieber J, Scheres B, Genschik P - PLoS Genet. (2009)

Bottom Line: This phenotype is suppressed by ethylene-insensitive or resistant mutations.Finally, we identify a function of CUL3 in distal root patterning, by a mechanism that is independent of ethylene.Thus, our work highlights that CUL3 is essential for the normal division and organisation of the root stem cell niche and columella root cap cells.

View Article: PubMed Central - PubMed

Affiliation: ZMBP-Developmental Genetics, Universität Tübingen, Tübingen, Germany.

ABSTRACT
CULLIN3 (CUL3) together with BTB-domain proteins form a class of Cullin-RING ubiquitin ligases (called CRL3s) that control the rapid and selective degradation of important regulatory proteins in all eukaryotes. Here, we report that in the model plant Arabidopsis thaliana, CUL3 regulates plant growth and development, not only during embryogenesis but also at post-embryonic stages. First, we show that CUL3 modulates the emission of ethylene, a gaseous plant hormone that is an important growth regulator. A CUL3 hypomorphic mutant accumulates ACS5, the rate-limiting enzyme in ethylene biosynthesis and as a consequence exhibits a constitutive ethylene response. Second, we provide evidence that CUL3 regulates primary root growth by a novel ethylene-dependant pathway. In particular, we show that CUL3 knockdown inhibits primary root growth by reducing root meristem size and cell number. This phenotype is suppressed by ethylene-insensitive or resistant mutations. Finally, we identify a function of CUL3 in distal root patterning, by a mechanism that is independent of ethylene. Thus, our work highlights that CUL3 is essential for the normal division and organisation of the root stem cell niche and columella root cap cells.

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Related in: MedlinePlus

The cul3hyp mutant exhibits the triple response in the dark.A. Phenotypes of 3-day-old etiolated seedlings of the indicated genotypes grown without ACC. B. Hypocotyl (light grey) and root (dark grey) length measurements of 3-day-old etiolated seedlings of the indicated genotypes grown without ACC. Values are average lengths (means±SD) of >30 hypocotyls or roots. T-tests were performed for each value compared to WT (the triple mutants were compared to their corresponding ethylene-insensitive mutants) indicating significant differences (p<0.05). The (*) symbol highlights values for which p>0.05.
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pgen-1000328-g002: The cul3hyp mutant exhibits the triple response in the dark.A. Phenotypes of 3-day-old etiolated seedlings of the indicated genotypes grown without ACC. B. Hypocotyl (light grey) and root (dark grey) length measurements of 3-day-old etiolated seedlings of the indicated genotypes grown without ACC. Values are average lengths (means±SD) of >30 hypocotyls or roots. T-tests were performed for each value compared to WT (the triple mutants were compared to their corresponding ethylene-insensitive mutants) indicating significant differences (p<0.05). The (*) symbol highlights values for which p>0.05.

Mentions: Because ETO1 is involved in the ethylene biosynthetic pathway and physically interacts with Arabidopsis CUL3A [20], most likely through its BTB domain, we investigated whether the cul3hyp mutant is affected in ethylene-mediated processes. In accordance with this speculation, etiolated cul3hyp mutants displayed a typical triple response in the absence of ethylene, which is characterized by short hypocotyls, short roots, and exaggerated apical hooks (Figure 2). The phenotype was similar to that of eto1-1, though less severe than the constitutive triple response1 (ctr1-1) mutant. It is noteworthy that the single cul3a-3 mutant displayed a weak triple response. Moreover, when germinated in the presence 5 µM ACC, the cul3hyp mutant was still responsive to ethylene in a root elongation assay (Figure S1).


Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms.

Thomann A, Lechner E, Hansen M, Dumbliauskas E, Parmentier Y, Kieber J, Scheres B, Genschik P - PLoS Genet. (2009)

The cul3hyp mutant exhibits the triple response in the dark.A. Phenotypes of 3-day-old etiolated seedlings of the indicated genotypes grown without ACC. B. Hypocotyl (light grey) and root (dark grey) length measurements of 3-day-old etiolated seedlings of the indicated genotypes grown without ACC. Values are average lengths (means±SD) of >30 hypocotyls or roots. T-tests were performed for each value compared to WT (the triple mutants were compared to their corresponding ethylene-insensitive mutants) indicating significant differences (p<0.05). The (*) symbol highlights values for which p>0.05.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2607017&req=5

pgen-1000328-g002: The cul3hyp mutant exhibits the triple response in the dark.A. Phenotypes of 3-day-old etiolated seedlings of the indicated genotypes grown without ACC. B. Hypocotyl (light grey) and root (dark grey) length measurements of 3-day-old etiolated seedlings of the indicated genotypes grown without ACC. Values are average lengths (means±SD) of >30 hypocotyls or roots. T-tests were performed for each value compared to WT (the triple mutants were compared to their corresponding ethylene-insensitive mutants) indicating significant differences (p<0.05). The (*) symbol highlights values for which p>0.05.
Mentions: Because ETO1 is involved in the ethylene biosynthetic pathway and physically interacts with Arabidopsis CUL3A [20], most likely through its BTB domain, we investigated whether the cul3hyp mutant is affected in ethylene-mediated processes. In accordance with this speculation, etiolated cul3hyp mutants displayed a typical triple response in the absence of ethylene, which is characterized by short hypocotyls, short roots, and exaggerated apical hooks (Figure 2). The phenotype was similar to that of eto1-1, though less severe than the constitutive triple response1 (ctr1-1) mutant. It is noteworthy that the single cul3a-3 mutant displayed a weak triple response. Moreover, when germinated in the presence 5 µM ACC, the cul3hyp mutant was still responsive to ethylene in a root elongation assay (Figure S1).

Bottom Line: This phenotype is suppressed by ethylene-insensitive or resistant mutations.Finally, we identify a function of CUL3 in distal root patterning, by a mechanism that is independent of ethylene.Thus, our work highlights that CUL3 is essential for the normal division and organisation of the root stem cell niche and columella root cap cells.

View Article: PubMed Central - PubMed

Affiliation: ZMBP-Developmental Genetics, Universität Tübingen, Tübingen, Germany.

ABSTRACT
CULLIN3 (CUL3) together with BTB-domain proteins form a class of Cullin-RING ubiquitin ligases (called CRL3s) that control the rapid and selective degradation of important regulatory proteins in all eukaryotes. Here, we report that in the model plant Arabidopsis thaliana, CUL3 regulates plant growth and development, not only during embryogenesis but also at post-embryonic stages. First, we show that CUL3 modulates the emission of ethylene, a gaseous plant hormone that is an important growth regulator. A CUL3 hypomorphic mutant accumulates ACS5, the rate-limiting enzyme in ethylene biosynthesis and as a consequence exhibits a constitutive ethylene response. Second, we provide evidence that CUL3 regulates primary root growth by a novel ethylene-dependant pathway. In particular, we show that CUL3 knockdown inhibits primary root growth by reducing root meristem size and cell number. This phenotype is suppressed by ethylene-insensitive or resistant mutations. Finally, we identify a function of CUL3 in distal root patterning, by a mechanism that is independent of ethylene. Thus, our work highlights that CUL3 is essential for the normal division and organisation of the root stem cell niche and columella root cap cells.

Show MeSH
Related in: MedlinePlus