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

Augustine, Robert C.; York, Samuel L; Rytz, Thérèse C.; Vierstra, R.D.

doi:10.1104/pp.16.00353

Cited by 60 publications

(82 citation statements)

References 88 publications

(172 reference statements)

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“…Notably, ZmSUMO1 was previously reported to use nearly all accessible Lys residues (Lys-9, Lys-10, Lys-21, Lys-23, Lys-41 and Lys-42) to assemble poly-SUMO chains in the E. coli system. 4 Conservation of the noncovalent interaction sites and Lys residues is reduced in other SUMO isoforms and nearly absent in ZmDSUL, suggesting diversification of SUMO-/DSUL-conjugation patterns and confirming the observation that there is almost no overlap between SUMO1 and DSUL targets of maize. 5 Phylogenetic and expression analyses further show that AtSUMO4, AtSUMO6-8 (transcriptionally inactive) and ZmSUMO-v (lacking the diGly motif necessary for conjugation) belong to the so-called non-functional PTMs (Figure 1(b)).…”

Section: Textsupporting

confidence: 67%

“…5 Phylogenetic and expression analyses further show that AtSUMO4, AtSUMO6-8 (transcriptionally inactive) and ZmSUMO-v (lacking the diGly motif necessary for conjugation) belong to the so-called non-functional PTMs (Figure 1(b)). 4 Functional PTMs are generated by transcriptionally active members of the SUMO family with obvious C-terminal diGly motifs present in AtSUMO1, AtSUMO2 and ZmSUMO1 that form their own clade, which is related to all human SUMOs. These likely represent the highly conserved and predominantly nuclear-localized isoforms in plants and they share largely overlapping substrates and similar subcellular localization patterns.…”

Section: Textmentioning

confidence: 99%

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Overexpression of SUMO1 located predominately to euchromatin of dividing cells affects reproductive development in maize

Chen

Müller

Wang

et al. 2019

Plant Signaling & Behavior

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Post-translational modification of proteins by small ubiquitin-like modifier (SUMO) plays essential roles in a large variety of cellular and developmental processes. While SUMO conjugation to target proteins has been reported in numerous studies in animals and human, and partly also in the model plant Arabidopsis, little is known about the specific roles of SUMO in crop plants. Here, we report about the maize SUMO family and show that the highly conserved core isoform SUMO1 predominately locates to the nucleus where it marks euchromatin rather than heterochromatin. Moreover, SUMO1 is especially present in nuclei of small dividing cells. Strong overexpression of SUMO1 caused a severe dwarf phenotype and abnormalities in floral organ structures. Defects in anther development and female gametogenesis occurred similar to null-mutant phenotypes reported in Arabidopsis . Taken together, these studies imply that precise and fine-tuned conjugation of the highly conserved plant SUMO1 isoform to target proteins is required for vegetative and reproductive development. Mis-regulation by overexpression or knock-out is deleterious, strongly affecting fertility in both dicots and monocots, including the crop plant maize.

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Section: Textsupporting

confidence: 67%

Section: Textmentioning

confidence: 99%

Overexpression of SUMO1 located predominately to euchromatin of dividing cells affects reproductive development in maize

Chen

Müller

Wang

et al. 2019

Plant Signaling & Behavior

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“…In Arabidopsis, only the SUMO E2 enzyme SCE1 was identified, but rice, poplar (Populus spp. ), tomato, sorghum (Sorghum bicolor), and maize (Zea mays) were found to encode multiple SUMO E2s based on their genome sequence (Novatchkova et al, 2012;Augustine et al, 2016). The biological significance of the multiple SUMO E2s that are predicted in many plants, especially crop genomes, is unknown at present.…”

Section: Discussionmentioning

confidence: 99%

A Subset of Ubiquitin-Conjugating Enzymes Is Essential for Plant Immunity

et al. 2016

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Of the three classes of enzymes involved in ubiquitination, ubiquitin-conjugating enzymes (E2) have been often incorrectly considered to play merely an auxiliary role in the process, and few E2 enzymes have been investigated in plants. To reveal the role of E2 in plant innate immunity, we identified and cloned 40 tomato genes encoding ubiquitin E2 proteins. Thioester assays indicated that the majority of the genes encode enzymatically active E2. Phylogenetic analysis classified the 40 tomato E2 enzymes into 13 groups, of which members of group III were found to interact and act specifically with AvrPtoB, a Pseudomonas syringae pv tomato effector that uses its ubiquitin ligase (E3) activity to suppress host immunity. Knocking down the expression of group III E2 genes in Nicotiana benthamiana diminished the AvrPtoB-promoted degradation of the Fen kinase and the AvrPtoB suppression of host immunity-associated programmed cell death. Importantly, silencing group III E2 genes also resulted in reduced pattern-triggered immunity (PTI). By contrast, programmed cell death induced by several effector-triggered immunity elicitors was not affected on group III-silenced plants. Functional characterization suggested redundancy among group III members for their role in the suppression of plant immunity by AvrPtoB and in PTI and identified UBIQUITIN-CONJUGATING11 (UBC11), UBC28, UBC29, UBC39, and UBC40 as playing a more significant role in PTI than other group III members. Our work builds a foundation for the further characterization of E2s in plant immunity and reveals that AvrPtoB has evolved a strategy for suppressing host immunity that is difficult for the plant to thwart.Ubiquitination as a major posttranslational modification of proteins in eukaryotes has emerged in recent years as an important regulatory mechanism underlying plant innate immunity Fu et al., 2012;Marino et al., 2012;Li et al., 2014). The ubiquitination process involves a consecutive, threestep enzymatic cascade that is catalyzed by three different classes of enzymes: ubiquitin-activating (E1), ubiquitin-conjugating (E2), and ubiquitin ligase (E3) enzymes. The first step of the process activates ubiquitin, a highly conserved 76-amino acid protein, in an ATP-dependent manner by attaching ubiquitin to an E1 enzyme. The activated ubiquitin is then transferred from the E1 to the Cys residue at the active site of an E2 conjugating enzyme. An E3 ligase then recruits the substrate protein to the E2 to transfer the ubiquitin molecule from E2 to the substrate. Through the action of E1, E2, and E3, ubiquitin is covalently attached usually to the Lys residue of a substrate through an isopeptide bond (Hershko and Ciechanover, 1998). Of the three enzymes involved in ubiquitination, E3 ubiquitin ligases have been the focus of many studies due to their key role in determining substrate specificity for the ubiquitination

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“…SUMOylation has been implicated in the regulation of developmental, hormonal, and environmental responses in Arabidopsis , such as gametophyte development (Ling et al ; Liu et al ), embryogenesis (Saracco et al ), photomorphogenesis (Sadanandom et al ; Lin et al ), flowering time (Murtas et al ; Jin et al ), cell proliferation (Huang et al ; Ishida et al ), abscisic acid (ABA) signaling (Miura et al ; Zheng et al ), gibberellic acid (GA) signaling (Kim et al ), the salt stress response (Conti et al ), thermal adaptation (Yoo et al ; Miura et al ), the drought stress response (Catala et al ; Zhang et al ), immune responses (Lee et al ; Saleh et al ), and nutrient (phosphate and nitrogen) starvation signaling (Miura et al ; Park et al ). The SUMO regulatory mechanism is conserved in Oryza sativa (rice), Zea mays (maize), Dendrobium (orchids), and Malus domestica (apple; Park et al ; Liu et al ; Augustine et al ; Zhang et al ). The SUMO E3 ligase OsSIZ1 regulates phosphate‐ and nitrogen‐dependent responses, spikelet fertility, and plant development in rice (Thangasamy et al ; Wang 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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Defining the SUMO System in Maize: SUMOylation Is Up-Regulated during Endosperm Development and Rapidly Induced by Stress

Cited by 60 publications

References 88 publications

Overexpression of SUMO1 located predominately to euchromatin of dividing cells affects reproductive development in maize

Overexpression of SUMO1 located predominately to euchromatin of dividing cells affects reproductive development in maize

A Subset of Ubiquitin-Conjugating Enzymes Is Essential for Plant Immunity

SUMO E3 Ligases GmSIZ1a and GmSIZ1b regulate vegetative growth in soybean

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