The Pleiotropic Role of the 26S Proteasome Subunit RPN10 in Arabidopsis Growth and Development Supports a Substrate-Specific Function in Abscisic Acid Signaling

Smalle, Jan; Kurepa, Jasmina; Yang, Peizhen; Emborg, Thomas J.; Babiychuk, Elena; Kushnir, Sergeï; Vierstra, Richard D.

doi:10.1105/tpc.009217

Cited by 243 publications

(277 citation statements)

References 64 publications

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“…5 F-H). Interestingly, the rpn10 and keg mutants, which stabilize the ABI5 protein, exhibit a decreased hypocotyl growth as well (34,35). Thus, ABA may enhance seedling light response and inhibit hypocotyl elongation, which may confer increased resistance to drought and other stresses.…”

Section: Discussionmentioning

confidence: 99%

Integration of light and abscisic acid signaling during seed germination and early seedling development

Hao

Zhang

Neff

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

265

256

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Seed germination is regulated by endogenous hormonal cues and external environmental stimuli such as water, low temperature, and light. After germination, the young seedling must rapidly establish its root system and the photoautotrophic capability appropriate to its surrounding environment. Light and the phytohormone abscisic acid (ABA) both regulate seed germination and seedling development, although how light and ABA signals are integrated at the molecular level is not understood. Here, we found that the previously described light-signaling component HY5 also mediates ABA response in seed germination, early seedling growth, and root development in Arabidopsis. HY5 binds to the promoter of the transcription factor ABI5 gene with high affinity and is required for the expression of ABI5 and ABI5-targeted late embryogenesis-abundant genes in seeds. Chromatin immunoprecipitation also indicated that the binding of HY5 to the ABI5 promoter is significantly enhanced by ABA. Overexpression of ABI5 restores ABA sensitivity in hy5 and results in enhanced light responses and shorter hypocotyls in the wild type. Our studies identified an unexpected mode of light and ABA signal integration that may help young seedlings better adapt to environmental stresses.light response ͉ signal transduction T he plant hormone abscisic acid (ABA) plays essential roles in several aspects of plant growth and development, including seed maturation, seed dormancy, and adaptation to environmental stresses such as drought and high salinity (1-4). Genetic studies of ABA regulation of seed germination and gene expression have identified a number of Arabidopsis mutants with altered ABA sensitivities. One of the ABA insensitive mutants, abi5, was isolated for its ability to germinate in the presence of higher concentrations of exogenous ABA (5). ABI5 encodes a basic leucine zipper (bZIP) transcription factor whose accumulation inhibits seed germination and early seedling establishment (6-8). ABI5 regulates the expression of ABA induced, mostly seed-specific, AtEM genes that encode class I late embryogenesis-abundant (LEA) proteins important for seed maturation (6, 9, 10). Interestingly, the ABI5 gene was also expressed in young seedlings, suggesting that ABI5 may have additional functions beyond seed development and germination (11). It is known that seed germination and early seedling development are also regulated by light (12). Yet little is known how light and ABA signals are integrated in the regulation of this common developmental transition from seeds to seedlings.Whereas the role of ABA in seedling photomorphogenesis is unclear, ABA is well recognized for its critical roles in plant adaptation to drought stress. In addition to inducing stomatal closure and the activation of stress-responsive genes, ABA was recently found to be involved in lateral root development (13-15). Genetic studies indicated that the inhibition of lateral root elongation and potential promotion of primary root growth by drought stress and ABA are adaptive responses o...

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Section: Discussionmentioning

confidence: 99%

Integration of light and abscisic acid signaling during seed germination and early seedling development

Hao

Zhang

Neff

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

265

256

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“…On the other hand, a mutation in the RPN10 gene results in a pleiotropic phenotype in Arabidopsis. The rpn10-1 mutant is more sensitive to ABA, salinity, Suc stress, and DNA-damaging agents, whereas the mutant is less responsive to cytokinin and auxin (Smalle et al, 2003). Peng et al (2001) found that the RPN6 protein, a non-ATPase regulatory subunit, exists in two distinct protein complexes of about 800 and 500 kD, respectively, in Arabidopsis and cauliflower (Brassica oleracea) plants.…”

Section: Discussionmentioning

confidence: 99%

Heterologous Expression and Molecular and Cellular Characterization of CaPUB1 Encoding a Hot Pepper U-Box E3 Ubiquitin Ligase Homolog

et al. 2006

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The U-box motif is a conserved domain found in the diverse isoforms of E3 ubiquitin ligase in eukaryotes. From water-stressed hot pepper (Capsicum annuum L. cv Pukang) plants, we isolated C. annuum putative U-box protein 1 (CaPUB1), which encodes a protein containing a single U-box motif in its N-terminal region. In vitro ubiquitination and site-directed mutagenesis assays revealed that CaPUB1 possessed E3 ubiquitin ligase activity and that the U-box motif was indeed essential for its enzyme activity. RNA gel-blot analysis showed that CaPUB1 mRNA was induced rapidly by a broad spectrum of abiotic stresses, including drought, high salinity, cold temperature, and mechanical wounding, but not in response to ethylene, abscisic acid, or a bacterial pathogen, suggesting its role in the early events in the abiotic-related defense response. Because transgenic work was extremely difficult in hot pepper, in this study we overexpressed CaPUB1 in Arabidopsis (Arabidopsis thaliana) to provide cellular information on the function of this gene in the development and plant responses to abiotic stresses. Transgenic Arabidopsis plants that constitutively expressed the CaPUB1 gene under the control of the cauliflower mosaic virus 35S promoter had markedly longer hypocotyls and roots and grew more rapidly than the wild type, leading to an early bolting phenotype. Microscopic analysis showed that 35STCaPUB1 roots had increased numbers of small-sized cells, resulting in disordered, highly populated cell layers in the cortex, endodermis, and stele. In addition, CaPUB1-overexpressing plants displayed increased sensitivity to water stress and mild salinity. These results indicate that CaPUB1 is functional in Arabidopsis cells, thereby effectively altering cell and tissue growth and also the response to abiotic stresses. Comparative proteomic analysis showed that the level of RPN6 protein, a non-ATPase subunit of the 26S proteasome complex, was significantly reduced in 35STCaPUB1 seedlings as compared to the wild type. Pull-down and ubiquitination assays demonstrated that RPN6 interacted physically with CaPUB1 and was ubiquitinated in a CaPUB1-dependent manner in vitro. Although the physiological function of CaPUB1 is not yet clear, there are several possibilities for its involvement in a subset of physiological responses to counteract dehydration and high-salinity stresses in transgenic Arabidopsis seedlings.

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“…Together, this suggests that the mature ovary before pollination has entered a temporarily dormant state, during which the tissue is quiescent. It is known that ABA can directly inXuence the cell cycle via suppression of CDKA1 expression (Smalle et al 2003) or stimulation of the ICK1 (an inhibitor of CDK action) expression (Wang et al 1998), thereby inhibiting cell division and inducing an quiescent state. We know that the ABA signaling and response pathway are active in the unpollinated mature ovary (Vriezen et al 2008).…”

Section: Function Of Aba During Fruit Setmentioning

confidence: 99%

Abscisic acid levels in tomato ovaries are regulated by LeNCED1 and SlCYP707A1

Nitsch

Oplaat

Feron

et al. 2009

Planta

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Although the hormones, gibberellin and auxin, are known to play a role in the initiation of fruits, no such function has yet been demonstrated for abscisic acid (ABA). However, ABA signaling and ABA responses are high in tomato (Solanum lycopersicum L.) ovaries before pollination and decrease thereafter (Vriezen et al. in New Phytol 177:60-76, 2008). As a Wrst step to understanding the role of ABA in ovary development and fruit set in tomato, we analyzed ABA content and the expression of genes involved in its metabolism in relation to pollination. We show that ABA levels are relatively high in mature ovaries and decrease directly after pollination, while an increase in the ABA metabolite dihydrophaseic acid was measured. An important regulator of ABA biosynthesis in tomato is 9-cis-epoxy-carotenoid dioxygenase (LeNCED1), whose mRNA level in ovaries is reduced after pollination. The increased catabolism is likely caused by strong induction of one of four newly identiWed putative (+)ABA 8Ј-hydroxylase genes. This gene was named SlCYP707A1 and is expressed speciWcally in ovules and placenta. Transgenic plants, overexpressing SlCYP707A1, have reduced ABA levels and exhibit ABA-deWcient phenotypes suggesting that this gene encodes a functional ABA 8Ј-hydroxylase. Gibberellin and auxin application have diVerent eVects on the LeNCED1 and SlCYP707A1 gene expression. The crosstalk between auxins, gibberellins and ABA during fruit set is discussed.

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The Pleiotropic Role of the 26S Proteasome Subunit RPN10 in Arabidopsis Growth and Development Supports a Substrate-Specific Function in Abscisic Acid Signaling

Cited by 243 publications

References 64 publications

Integration of light and abscisic acid signaling during seed germination and early seedling development

Integration of light and abscisic acid signaling during seed germination and early seedling development

Heterologous Expression and Molecular and Cellular Characterization of CaPUB1 Encoding a Hot Pepper U-Box E3 Ubiquitin Ligase Homolog

Abscisic acid levels in tomato ovaries are regulated by LeNCED1 and SlCYP707A1

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