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Disturbed local auxin homeostasis enhances cellular anisotropy and reveals alternative wiring of auxin-ethylene crosstalk in Brachypodium distachyon seminal roots.

ABSTRACT: Observations gained from model organisms are essential, yet it remains unclear to which degree they are applicable to distant relatives. For example, in the dicotyledon Arabidopsis thaliana (Arabidopsis), auxin biosynthesis via indole-3-pyruvic acid (IPA) is essential for root development and requires redundant TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) and TAA1-RELATED (TAR) genes. A promoter T-DNA insertion in the monocotyledon Brachypodium distachyon (Brachypodium) TAR2-LIKE gene (BdTAR2L) severely down-regulates expression, suggesting reduced tryptophan aminotransferase activity in this mutant, which thus represents a hypomorphic Bdtar2l allele (Bdtar2l(hypo) ). Counterintuitive however, Bdtar2l(hypo) mutants display dramatically elongated seminal roots because of enhanced cell elongation. This phenotype is also observed in another, stronger Bdtar2l allele and can be mimicked by treating wild type with L-kynerunine, a specific TAA1/TAR inhibitor. Surprisingly, L-kynerunine-treated as well as Bdtar2l roots display elevated rather than reduced auxin levels. This does not appear to result from compensation by alternative auxin biosynthesis pathways. Rather, expression of YUCCA genes, which are rate-limiting for conversion of IPA to auxin, is increased in Bdtar2l mutants. Consistent with suppression of Bdtar2l(hypo) root phenotypes upon application of the ethylene precursor 1-aminocyclopropane-1-carboxylic-acid (ACC), BdYUCCA genes are down-regulated upon ACC treatment. Moreover, they are up-regulated in a downstream ethylene-signaling component homolog mutant, Bd ethylene insensitive 2-like 1, which also displays a Bdtar2l root phenotype. In summary, Bdtar2l phenotypes contrast with gradually reduced root growth and auxin levels described for Arabidopsis taa1/tar mutants. This could be explained if in Brachypodium, ethylene inhibits the rate-limiting step of auxin biosynthesis in an IPA-dependent manner to confer auxin levels that are sub-optimal for root cell elongation, as suggested by our observations. Thus, our results reveal a delicate homeostasis of local auxin and ethylene activity to control cell elongation in Brachypodium roots and suggest alternative wiring of auxin-ethylene crosstalk as compared to Arabidopsis.

SUBMITTER: Pacheco-Villalobos D

PROVIDER: S-EPMC3688705 | biostudies-literature | 2013 Jun

REPOSITORIES: biostudies-literature

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Disturbed local auxin homeostasis enhances cellular anisotropy and reveals alternative wiring of auxin-ethylene crosstalk in Brachypodium distachyon seminal roots.

Pacheco-Villalobos David D Sankar Martial M Ljung Karin K Hardtke Christian S CS

PLoS genetics 20130620 6

Observations gained from model organisms are essential, yet it remains unclear to which degree they are applicable to distant relatives. For example, in the dicotyledon Arabidopsis thaliana (Arabidopsis), auxin biosynthesis via indole-3-pyruvic acid (IPA) is essential for root development and requires redundant TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) and TAA1-RELATED (TAR) genes. A promoter T-DNA insertion in the monocotyledon Brachypodium distachyon (Brachypodium) TAR2-LIKE gene (Bd ...[more]

PMID: 23840182

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Project description:Fruit ripening is a highly coordinated developmental process driven by a complex hormonal network. Ethylene is the main regulator of climacteric fruit ripening. However, a putative role of other key phytohormones in this process cannot be excluded. We previously observed an increasing level of auxin during the post-harvest ripening of the durian fruit, which occurred concomitantly with the rise in the climacteric ethylene biosynthesis. Herein, we connect the key auxin signaling component, auxin response factors (ARFs), with the regulatory network that controls fruit ripening in durian through the identification and functional characterization of a candidate ripening-associated ARF. Our transcriptome-wide analysis identified 15 ARF members in durian (DzARFs), out of which 12 were expressed in the fruit pulp. Most of these DzARFs showed a differential expression, but DzARF2A had a marked ripening-associated expression pattern during post-harvest ripening in Monthong, a commercial durian cultivar from Thailand. Phylogenetic analysis of DzARF2A based on its tomato orthologue predicted a role in ripening through the regulation of ethylene biosynthesis. Transient expression of DzARF2A in Nicotiana benthamiana leaves significantly upregulated the expression levels of ethylene biosynthetic genes, pointing to a ripening-associated role of DzARF2A through the transcriptional regulation of ethylene biosynthesis. Dual-luciferase reporter assay determined that DzARF2A trans-activates durian ethylene biosynthetic genes. We previously reported significantly higher auxin level during post-harvest ripening in a fast-ripening cultivar (Chanee) compared to a slow-ripening one (Monthong). DzARF2A expression was significantly higher during post-harvest ripening in the fast-ripening cultivars (Chanee and Phuangmanee) compared to that of the slow-ripening ones (Monthong and Kanyao). Thus, higher auxin level could upregulate the expression of DzARF2A during ripening of a fast-ripening cultivar. The auxin-induced expression of DzARF2A confirmed its responsiveness to exogenous auxin treatment in a dose-dependent manner, suggesting an auxin-mediated role of DzARF2A in fruit ripening. We suggest that high DzARF2A expression would activate ARF2A-mediated transcription of ethylene biosynthetic genes, leading to increased climacteric ethylene biosynthesis (auxin-ethylene crosstalk) and faster ripening. Hence, we demonstrated DzARF2A as a new component of the regulatory network possibly mediating durian fruit ripening through transcriptional regulation of ethylene biosynthetic genes.

Dataset Information

Disturbed local auxin homeostasis enhances cellular anisotropy and reveals alternative wiring of auxin-ethylene crosstalk in Brachypodium distachyon seminal roots.

Publications

Disturbed local auxin homeostasis enhances cellular anisotropy and reveals alternative wiring of auxin-ethylene crosstalk in Brachypodium distachyon seminal roots.

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