Protein post-translational modifications diversify the proteome and install new regulatory levels that are crucial for the maintenance of cellular homeostasis. Over the last decade, the ubiquitin-like modifying peptide small ubiquitin-like modifier (SUMO) has been shown to regulate various nuclear processes, including transcriptional control. In plants, the sumoylation pathway has been significantly implicated in the response to environmental stimuli, including heat, cold, drought, and salt stresses, modulation of abscisic acid and other hormones, and nutrient homeostasis. This review focuses on the emerging importance of SUMO in the abiotic stress response, summarizing the molecular implications of sumoylation and emphasizing how high-throughput approaches aimed at identifying the full set of SUMO targets will greatly enhance our understanding of the SUMO-abiotic stress association.
Zinc (Zn) is an essential micronutrient for plants and animals because of its structural and catalytic roles in many proteins. Zn deficiency affects ca. two billion people, mainly those living on plant-based diets that rely on crops from Zn deficient soils. Plants maintain adequate Zn levels through tightly regulated Zn homeostasis mechanisms, involving Zn uptake, distribution and storage, but it was not known how they sense Zn status. We use in vitro and in planta approaches to show that the Arabidopsis thaliana F-group bZIP transcription factors bZIP19 and bZIP23, which are the central regulators of the Zn deficiency response, act as Zn sensors by binding Zn 2+ ions to a Zn sensor motif (ZSM).Deletions or modifications of this ZSM disrupts Zn binding, leading to a constitutive transcriptional Zn deficiency response, which causes a significant increase in plant and seed Zn accumulation. Since the ZSM is highly conserved in F-bZIPs across land plants, the identification of the first plant Zn-sensor will promote new strategies to improve the Zn nutritional quality of plant-derived food and feed, and contribute to tackle the global Zn deficiency health problem.
Abstract. 1. A thorough inventory of a Mediterranean oak forest spider fauna carried out during 2 weeks is presented. It used a semi-quantitative sampling protocol to collect comparable data in a rigorous, rapid and efficient way. Four hundred and eighty samples of one person-hour of work each were collected, mostly inside a delimited 1-ha plot.2. Sampling yielded 10 808 adult spiders representing 204 species. The number of species present at the site was estimated using five different richness estimators (Chao1, Chao2, Jackknife1, Jackknife2 and Michaelis-Menten). The estimates ranged from 232 to 260. The most reliable estimates were provided by the Chao estimators and the least reliable was obtained with the Michaelis-Menten. However, the behavior of the Michaelis-Menten accumulation curves supports the use of this estimator as a stopping or reliability rule.3. Nineteen per cent of the species were represented by a single specimen (singletons) and 12% by just two specimens (doubletons). The presence of locally rare species in this exhaustive inventory is discussed.4. The effects of day, time of day, collector experience and sampling method on the number of adults, number of species and taxonomic composition of the samples are assessed. Sampling method is the single most important factor influencing the results and all methods generate unique species. Time of day is also important, in such way that each combination of method and time of day may be considered as a different method in itself. There are insignificant differences between the collectors in terms of species and number of adult spiders collected. Despite the high collecting effort, the species richness and abundance of spiders remained constant throughout the sampling period.
Basic leucine zipper (bZIP) transcription factors control important developmental and physiological processes in plants. In Arabidopsis thaliana, the three gene F-bZIP subfamily has been associated with zinc deficiency and salt stress response. Benefiting from the present abundance of plant genomic data, we performed an evolutionary and structural characterization of plant F-bZIPs. We observed divergence during seed plant evolution, into two groups and inferred different selective pressures for each. Group 1 contains AtbZIP19 and AtbZIP23 and appears more conserved, whereas Group 2, containing AtbZIP24, is more prone to gene loss and expansion events. Transcriptomic and experimental data reinforced AtbZIP19/23 as pivotal regulators of the zinc deficiency response, mostly via the activation of genes from the ZIP metal transporter family, and revealed that they are the main regulatory switch of AtZIP4. A survey of AtZIP4 orthologs promoters across different plant taxa revealed an enrichment of the Zinc Deficiency Response Element (ZDRE) to which both AtbZIP19/23 bind. Overall, our results indicate that while the AtbZIP24 function in the regulation of the salt stress response may be the result of neo-functionalization, the AtbZIP19/23 function in the regulation of the zinc deficiency response may be conserved in land plants (Embryophytes).
The F-bZIP transcription factors bZIP19 and bZIP23 are the central regulators of the zinc deficiency response in Arabidopsis, and phylogenetic analysis of F-bZIP homologs across land plants indicates that the regulatory mechanism of the zinc deficiency response may be conserved. Here, we identified the rice F-bZIP homologs and investigated their function. OsbZIP48 and OsbZIP50, but not OsbZIP49, complement the zinc deficiency-hypersensitive Arabidopsis bzip19bzip23 double mutant. Ectopic expression of OsbZIP50 in Arabidopsis significantly increases plant zinc accumulation under control zinc supply, suggesting an altered Zn sensing in OsbZIP50. In addition, we performed a phylogenetic analysis of F-bZIP homologs from representative monocot species that supports the branching of plant F-bZIPs into Group 1 and Group 2. Our results suggest that regulation of the zinc deficiency response in rice is conserved, with OsbZIP48 being a functional homolog of AtbZIP19 and AtbZIP23. A better understanding of the mechanisms behind the Zn deficiency response in rice and other important crops will contribute to develop plant-based strategies to address the problems of Zn deficiency in soils, crops, and cereal-based human diets.
All living organisms require zinc as an essential micronutrient. Maintaining appropriate intracellular zinc supply, and avoiding deficiency or toxic excess, requires a tight regulation of zinc homeostasis. In Arabidopsis, bZIP19 and bZIP23 (basic-leucine zipper) transcription factors are the central regulators of the zinc deficiency response. Their targets include members of the ZIP (Zrt/Irt-like Protein) transporter family, involved in cellular zinc uptake, which are up-regulated at zinc deficiency. However, the mechanisms by which these transcription factors are regulated by cellular zinc status are not yet known. Here, to further our insight, we took advantage of the zinc deficiency hypersensitive phenotype of the bzip19 bzip23 double mutant, and used it as background to produce complementation lines of each Arabidopsis F-bZIP transcription factor, including bZIP24. On these lines, we performed complementation and localization studies, analyzed the transcript level of a subset of putative target genes, and performed elemental tissue profiling. We find evidence supporting that the zinc-dependent activity of bZIP19 and bZIP23 is modulated by zinc at protein level, in the nucleus, where cellular zinc sufficiency represses their activity and zinc deficiency is required. In addition, we show that these two transcription factors are functionally redundant to a large extent, and that differential tissue-specific expression patterns might, at least partly, explain distinct regulatory activities. Finally, we show that bZIP24 does not play a central role in the Zn deficiency response. Overall, we provide novel information that advances our understanding of the regulatory activity of bZIP19 and bZIP23.
Sumoylation is an essential post-translational regulator of plant development and the response to environmental stimuli. SUMO conjugation occurs via an E1-E2-E3 cascade, and can be removed by SUMO proteases (ULPs). ULPs are numerous and likely to function as sources of specificity within the pathway, yet most ULPs remain functionally unresolved. In this report we used loss-of-function reverse genetics and transcriptomics to functionally characterize Arabidopsis thaliana ULP1c and ULP1d SUMO proteases. GUS reporter assays implicated ULP1c/d in various developmental stages, and subsequent defects in growth and germination were uncovered using loss-of-function mutants. Microarray analysis evidenced not only a deregulation of genes involved in development, but also in genes controlled by various drought-associated transcriptional regulators. We demonstrated that ulp1c ulp1d displayed diminished in vitro root growth under low water potential and higher stomatal aperture, yet leaf transpirational water loss and whole drought tolerance were not significantly altered. Generation of a triple siz1 ulp1c ulp1d mutant suggests that ULP1c/d and the SUMO E3 ligase SIZ1 may display separate functions in development yet operate epistatically in response to water deficit. We provide experimental evidence that Arabidopsis ULP1c and ULP1d proteases act redundantly as positive regulators of growth, and operate mainly as isopeptidases downstream of SIZ1 in the control of water deficit responses.
Post-translational modification mechanisms function as switches that mediate the balance between optimum growth and the response to environmental stimuli, by regulating the activity of key proteins. SUMO (small ubiquitin-like modifier) attachment, or sumoylation, is a post-translational modification that is essential for the plant stress response, also modulating hormonal circuits to co-ordinate developmental processes. The Arabidopsis SUMO E3 ligase SAP and Miz 1 (SIZ1) is the major SUMO conjugation enhancer in response to stress, and is implicated in several aspects of plant development. Here we report that known SUMO targets are over-represented in multiple carbohydrate-related proteins, suggesting a functional link between sumoylation and sugar metabolism and signaling in plants. We subsequently observed that SUMO-conjugated proteins accumulate in response to high doses of sugar in a SIZ1-dependent manner, and that the null siz1 mutant displays increased expression of sucrose and starch catabolic genes and shows reduced starch levels. We demonstrated that SIZ1 controls germination time and post-germination growth via osmotic and sugar-dependent signaling, respectively. Glucose was specifically linked to SUMO-sugar interplay, with high levels inducing root growth inhibition and aberrant root hair morphology in siz1. The use of sugar analogs and sugar marker gene expression analysis allowed us to implicate SIZ1 in a signaling pathway dependent on glucose metabolism, probably involving modulation of SNF1-related kinase 1 (SnRK1) activity.
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