SUMO Is a Critical Regulator of Salt Stress Responses in Rice

Srivastava, Anjil Kumar; Zhang, Cunzin; Yates, Gary; Bailey, Mark; Brown, Adrian P.; Sadanandom, Ari

doi:10.1104/pp.15.01530

Cited by 65 publications

(68 citation statements)

References 58 publications

(74 reference statements)

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“…Previously we revealed in rice the SUMO protease gene family and showed that OsOTS1 has a key role in tolerance to high salinity (Srivastava et al ., ). Here, we report that drought stress and ABA stimulates the degradation of OsOTS1 protein.…”

Section: Introductionmentioning

confidence: 97%

RiceSUMOproteaseOverly Tolerant to Salt 1targets the transcription factor, OsbZIP23 to promote drought tolerance in rice

et al. 2017

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Conjugation of SUMO (Small Ubiquitin-like Modifier) protein to cellular targets is emerging as a very influential protein modification system. Once covalently bound, SUMO conjugation can change the stability or functionality of its cognate target proteins. SUMO protease can rapidly reverse SUMO conjugation making this modification system highly dynamic. A major factor in the variation of SUMO-target function is the balance between the conjugated/de-conjugated forms. The mechanistic role of these regulatory SUMO proteases in mediating stress responses has not been defined in any crops. In this study, we reveal the role of the SUMO protease, OsOTS1 in mediating tolerance to drought in rice. OsOTS1 depleted transgenic plants accumulate more ABA and exhibit more productive agronomic traits during drought while OsOTS1 overexpressing lines are drought sensitive but ABA insensitive. Drought and ABA treatment stimulates the degradation of OsOTS1 protein indicating that SUMO conjugation is an important response to drought stress in rice achieved through down-regulation of OTS1/2 activity. We reveal that OsOTS1 SUMO protease directly targets the ABA and drought responsive transcription factor OsbZIP23 for de-SUMOylation affecting its stability. OsOTS-RNAi lines show increased abundance of OsbZIP23 and increased drought responsive gene expression while OsOTS1 overexpressing lines show reduced levels of OsbZIP23 leading to suppressed drought responsive gene expression. Our data reveal a mechanism in which rice plants govern ABA-dependant drought responsive gene expression by controlling the stability of OsbZIP23 by SUMO conjugation through manipulating specific SUMO protease levels.

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Section: Introductionmentioning

confidence: 97%

RiceSUMOproteaseOverly Tolerant to Salt 1targets the transcription factor, OsbZIP23 to promote drought tolerance in rice

et al. 2017

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“…The SUMO E3 ligase OsSIZ1 regulates phosphate‐ and nitrogen‐dependent responses, spikelet fertility, and plant development in rice (Thangasamy et al ; Wang et al , ). Moreover, the OsOTS1 SUMO protease positively regulates salt stress responses in rice (Srivastava et al ). Mutations in an Arabidopsis SUMO E3 ligase, AtSIZ1 , increase salicylic acid (SA) levels, resulting in reduced plant stature, constitutively activated immune responses, and early flowering (Lee et al ; Jin et al ; Miura et al ).…”

Section: Introductionmentioning

confidence: 99%

SUMO E3 Ligases GmSIZ1a and GmSIZ1b regulate vegetative growth in soybean

Cai

Kong

Zhong

et al. 2017

JIPB

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SIZ1 is a small ubiquitin‐related modifier (SUMO) E3 ligase that mediates post‐translational SUMO modification of target proteins and thereby regulates developmental processes and hormonal and environmental stress responses in Arabidopsis. However, the role of SUMO E3 ligases in crop plants is largely unknown. Here, we identified and characterized two Glycine max (soybean) SUMO E3 ligases, GmSIZ1a and GmSIZ1b. Expression of GmSIZ1a and GmSIZ1b was induced in response to salicylic acid (SA), heat, and dehydration treatment, but not in response to cold, abscisic acid (ABA), and NaCl treatment. Although GmSIZ1a was expressed at higher levels than GmSIZ1b, both genes encoded proteins with SUMO E3 ligase activity in vivo. Heterologous expression of GmSIZ1a or GmSIZ1b rescued the mutant phenotype of Arabidopsis siz1‐2, including dwarfism, constitutively activated expression of pathogen‐related genes, and ABA‐sensitive seed germination. Simultaneous downregulation of GmSIZ1a and GmSIZ1b (GmSIZ1a/b) using RNA interference (RNAi)‐mediated gene silencing decreased heat shock‐induced SUMO conjugation in soybean. Moreover, GmSIZ1RNAi plants exhibited reduced plant height and leaf size. However, unlike Arabidopsis siz1‐2 mutant plants, flowering time and SA levels were not significantly altered in GmSIZ1RNAi plants. Taken together, our results indicate that GmSIZ1a and GmSIZ1b mediate SUMO modification and positively regulate vegetative growth in soybean.

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“…Rice siz1 alleles that attenuate SUMOylation have a smaller stature with a reduced root system, greater tillering, and reduced fecundity (Thangasamy et al, 2011) and accumulate higher levels of nitrogen and phosphorous, possibly due to the altered expression of genes involved in nutrient uptake (Wang et al, 2015). Conversely, OTS1 overexpression rendered rice resistant to high salt, whereas RNA interference-mediated silencing enhanced salt sensitivity (Srivastava et al, 2016). In addition, significant differences between the monocot and dicot SUMO systems have been observed.…”

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confidence: 99%

Defining the SUMO System in Maize: SUMOylation Is Up-Regulated during Endosperm Development and Rapidly Induced by Stress

et al. 2016

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In response to abiotic and biotic challenges, plants rapidly attach small ubiquitin-related modifier (SUMO) to a large collection of nuclear proteins, with studies in Arabidopsis (Arabidopsis thaliana) linking SUMOylation to stress tolerance via its modification of factors involved in chromatin and RNA dynamics. Despite this importance, little is known about SUMOylation in crop species. Here, we describe the plant SUMO system at the phylogenetic, biochemical, and transcriptional levels with a focus on maize (Zea mays). In addition to canonical SUMOs, land plants encode a loosely constrained noncanonical isoform and a variant containing a long extension upstream of the signature b-grasp fold, with cereals also expressing a novel diSUMO polypeptide bearing two SUMO b-grasp domains in tandem. Maize and other cereals also synthesize a unique SUMO-conjugating enzyme variant with more restricted expression patterns that is enzymatically active despite a distinct electrostatic surface. Maize SUMOylation primarily impacts nuclear substrates, is strongly induced by high temperatures, and displays a memory that suppresses subsequent conjugation. Both in-depth transcript and conjugate profiles in various maize organs point to tissue/cell-specific functions for SUMOylation, with potentially significant roles during embryo and endosperm maturation. Collectively, these studies define the organization of the maize SUMO system and imply important functions during seed development and stress defense.

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SUMO Is a Critical Regulator of Salt Stress Responses in Rice

Cited by 65 publications

References 58 publications

RiceSUMOproteaseOverly Tolerant to Salt 1targets the transcription factor, OsbZIP23 to promote drought tolerance in rice

RiceSUMOproteaseOverly Tolerant to Salt 1targets the transcription factor, OsbZIP23 to promote drought tolerance in rice

SUMO E3 Ligases GmSIZ1a and GmSIZ1b regulate vegetative growth in soybean

Defining the SUMO System in Maize: SUMOylation Is Up-Regulated during Endosperm Development and Rapidly Induced by Stress

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