Adaptive and degenerative evolution of the<i>S-Phase Kinase-Associated Protein 1-Like</i>family in<i>Arabidopsis thaliana</i>

Hua, Zhihua; Gao, Zhenyu

doi:10.7717/peerj.6740

Cited by 7 publications

(19 citation statements)

References 49 publications

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“…For example, the list of E3 ligases encoded in the genome of Arabidopsis thaliana , a model plant, contains over 1300 members (Vierstra, 2009; Hua and Yu, 2019). The large expansion of the E3 ligase group is consistent with its roles in plant adaptation (Hua and Gao, 2019; Hua and Yu, 2019).…”

Section: Introductionsupporting

confidence: 54%

“…Unfortunately, due to the varied effects of mutant alleles and their different genetic backgrounds ( axr6‐3 , cul1‐6 , and cul1‐7 are in Col‐0, icul3 is in Enkheim‐2 [En‐2], and cul‐494 is in Wassilewskija 4 [Ws‐4]), these mutants also showed several phenotypic differences, leaving the comprehensive functions of Cullin1 and SCF complexes unreconciled (Moon et al ., 2007; Gilkerson et al ., 2009; Pacurar et al ., 2014). Through genomic and evolutionary studies, we discovered that both FBX and ASK families showed significant sequence polymorphisms and diverse expression patterns across Arabidopsis populations, which indicates adaptive roles of SCF in different individuals (Hua et al ., 2013; Hua and Gao, 2019). Such natural variations further complicate the systematic understanding of SCF functions through mutagenesis analysis in different accessions.…”

Section: Introductionmentioning

confidence: 99%

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Generation of a fertile ask1 mutant uncovers a comprehensive set of SCF‐mediated intracellular functions

Yapa

Liao

et al. 2020

The Plant Journal

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Many eukaryotic intracellular processes employ protein ubiquitylation by ubiquitin E3 ligases for functional regulation or protein quality control. In plants, the multi-subunit Skp1-Cullin1-F-box (SCF) complexes compose the largest group of E3 ligases whose specificity is determined by a diverse array of F-box proteins. Although both sequence divergence and polymorphism of F-box genes well support a broad spectrum of SCF functions, experimental evidence is scarce due to the low number of identified SCF substrates. Taking advantage of the bridge role of Skp1 between F-box and Cullin1 in the complex, we systematically analyzed the functional influence of a well-characterized Arabidopsis Skp1-Like1 (ASK1) Ds insertion allele, ask1, in different Arabidopsis accessions. Through 10 generations of backcrossing with Columbia-0 (Col-0), we partially rescued the fertility of this otherwise sterile ask1 allele in Landsberg erecta, thus providing experimental evidence showing the polymorphic roles of SCF complexes. This ask1 mutant produces twisted rosette leaves, a reduced number of petals, fewer viable pollen grains, and larger embryos and seeds compared to Col-0. RNA-Seq-based transcriptome analysis of ask1 uncovered a large spectrum of SCF functions, which is greater than a 10-fold increase compared with previous studies. We also identified its hyposensitive responses to auxin and abscisic acid treatments and enhanced far-red light/phyA-mediated photomorphogenesis. Such diverse roles are consistent with the 20-30% reduction of ubiquitylation events in ask1 estimated by immunoblotting analysis in this work. Collectively, we conclude that ASK1 is a predominant Skp1 protein in Arabidopsis and that the fertile ask1 mutant allowed us to uncover a comprehensive set of SCF functions.

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Section: Introductionsupporting

confidence: 54%

Section: Introductionmentioning

confidence: 99%

Generation of a fertile ask1 mutant uncovers a comprehensive set of SCF‐mediated intracellular functions

Yapa

Liao

et al. 2020

The Plant Journal

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“…Relaxed negative selection may indicate a trend of neutralization. To test this hypothesis, we examined the neutral evolution of a UPS gene using the same approach employed previously to identify neutral changes of the Arabidopsis Skp1-like (ASK) genes [41]. By comparing the likelihood ratio obtained from two runs of codeml program with both fixed and free K a / K s ratios from the PAML4 package [40], we identified in total 113 out of 987 UPS genes (11.4%) that are under neutral changes in Aly .…”

Section: Resultsmentioning

confidence: 99%

“…Tandem duplications and retrotranspostion have been found to play a key role in the recent expansion of the ASK ( Skp1 ) family in Ath and the Ubiquiton family in 50 plant genomes [18,41], both of which belong to the ubiquitylation system. We next asked whether these two duplication mechanisms have also contributed to the differential expansion and diverse selection patterns of the UPS gene families across Brassicaceae and Poaceae species.…”

Section: Resultsmentioning

confidence: 99%

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Diversifying Evolution of the Ubiquitin-26S Proteasome System in Brassicaceae and Poaceae

Hua

2019

IJMS

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: Genome amplification and sequence divergence provides raw materials to allow organismal adaptation. This is exemplified by the large expansion of the ubiquitin-26S proteasome system (UPS) in land plants, which primarily rely on intracellular signaling and biochemical metabolism to combat biotic and abiotic stresses. While a handful of functional genomic studies have demonstrated the adaptive role of the UPS in plant growth and development, many UPS members remain unknown. In this work, we applied a comparative genomic study to address the functional divergence of the UPS at a systematic level. We first used a closing-target-trimming annotation approach to identify most, if not all, UPS members in six species from each of two evolutionarily distant plant families, Brassicaceae and Poaceae. To reduce age-related errors, the two groups of species were selected based on their similar chronological order of speciation. Through size comparison, chronological expansion inference, evolutionary selection analyses, duplication mechanism prediction, and functional domain enrichment assays, we discovered significant diversities within the UPS, particularly between members from its three largest ubiquitin ligase gene families, the F-box (FBX), the Really Interesting New Gene (RING), and the Bric-a-Brac/Tramtrack/Broad Complex (BTB) families, between Brassicaceae and Poaceae. Uncovering independent Arabidopsis and Oryza genus–specific subclades of the 26S proteasome subunits from a comprehensive phylogenetic analysis further supported a diversifying evolutionary model of the UPS in these two genera, confirming its role in plant adaptation.

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Dynamic interactions between SPX proteins, the ubiquitination machinery, and signalling molecules for stress adaptation at a whole-plant level

Collins,

Shou,

Mao

et al. 2024

Biochemical Journal

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The plant macronutrient phosphorus is a scarce resource and plant-available phosphate is limiting in most soil types. Generally, a gene regulatory module called the phosphate starvation response (PSR) enables efficient phosphate acquisition by roots and translocation to other organs. Plants growing on moderate to nutrient-rich soils need to co-ordinate availability of different nutrients and repress the highly efficient PSR to adjust phosphate acquisition to the availability of other macro- and micronutrients, and in particular nitrogen. PSR repression is mediated by a small family of single SYG1/Pho81/XPR1 (SPX) domain proteins. The SPX domain binds higher order inositol pyrophosphates that signal cellular phosphorus status and modulate SPX protein interaction with PHOSPHATE STARVATION RESPONSE1 (PHR1), the central transcriptional regulator of PSR. Sequestration by SPX repressors restricts PHR1 access to PSR gene promoters. Here we focus on SPX4 that primarily acts in shoots and sequesters many transcription factors other than PHR1 in the cytosol to control processes beyond the classical PSR, such as nitrate, auxin, and jasmonic acid signalling. Unlike SPX1 and SPX2, SPX4 is subject to proteasomal degradation not only by singular E3 ligases, but also by SCF–CRL complexes. Emerging models for these different layers of control and their consequences for plant acclimation to the environment will be discussed.

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Adaptive and degenerative evolution of theS-Phase Kinase-Associated Protein 1-Likefamily inArabidopsis thaliana

Cited by 7 publications

References 49 publications

Generation of a fertile ask1 mutant uncovers a comprehensive set of SCF‐mediated intracellular functions

Generation of a fertile ask1 mutant uncovers a comprehensive set of SCF‐mediated intracellular functions

Diversifying Evolution of the Ubiquitin-26S Proteasome System in Brassicaceae and Poaceae

Dynamic interactions between SPX proteins, the ubiquitination machinery, and signalling molecules for stress adaptation at a whole-plant level

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