Parasitic modulation of host development by ubiquitin-independent protein degradation

Huang, Weijie; MacLean, Allyson M.; Sugio, Akiko; Maqbool, Abbas; Busscher, Marco; Cho, Shu-Ting; Kamoun, Sophien; Kuo, Chih-Horng; Immink, Richard G. H.; Hogenhout, Saskia A.

doi:10.1016/j.cell.2021.08.029

Cited by 95 publications

(110 citation statements)

References 75 publications

(113 reference statements)

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“…Comparison of putative effector gene content revealed that ‘ Ca . P. aurantifolia’ NCHU2014 harbors SAP11 ( Bai et al, 2009 ) and SAP54 ( MacLean et al, 2011 ) homologs while lacking homologs o SAP05 ( Huang et al, 2021 ) or TENGU ( Hoshi et al, 2009 ; Figure 7 and Supplementary Table 2 ).…”

Section: Resultsmentioning

confidence: 99%

Accelerating Complete Phytoplasma Genome Assembly by Immunoprecipitation-Based Enrichment and MinION-Based DNA Sequencing for Comparative Analyses

et al. 2021

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Phytoplasmas are uncultivated plant-pathogenic bacteria with agricultural importance. Those belonging to the 16SrII group, represented by ‘Candidatus P. aurantifolia’, have a wide range of plant hosts and cause significant yield losses in valuable crops, such as pear, sweet potato, peanut, and soybean. In this study, a method that combines immunoprecipitation-based enrichment and MinION long-read DNA sequencing was developed to solve the challenge of phytoplasma genome studies. This approach produced long reads with high mapping rates and high genomic coverage that can be combined with Illumina reads to produce complete genome assemblies with high accuracy. We applied this method to strain NCHU2014 and determined its complete genome sequence, which consists of one circular chromosome with 635,584 bp and one plasmid with 4,224 bp. Although ‘Ca. P. aurantifolia’ NCHU2014 has a small chromosome with only 471 protein-coding genes, it contains 33 transporter genes and 27 putative effector genes, which may contribute to obtaining nutrients from hosts and manipulating host developments for their survival and multiplication. Two effectors, the homologs of SAP11 and SAP54/PHYL1 identified in ‘Ca. P. aurantifolia’ NCHU2014, have the biochemical activities in destabilizing host transcription factors, which can explain the disease symptoms observed in infected plants. Taken together, this study provides the first complete genome available for the 16SrII phytoplasmas and contributes to the understanding of phytoplasma pathogenicity.

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Section: Resultsmentioning

confidence: 99%

Accelerating Complete Phytoplasma Genome Assembly by Immunoprecipitation-Based Enrichment and MinION-Based DNA Sequencing for Comparative Analyses

et al. 2021

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“…In this study, protein degradation analysis revealed that MG132, a specific 26S proteasome, relieved the decrease level of ABI4 protein, indicating that ABI4 degradation was also regulated via the 26S proteasome pathway, which was also found in ABI1 and ABI5 [32,33]. However, a recent study has found that phytoplasma SAP05 (secreted AY-WB proteins) mediates the concurrent degradation of SPL and GATA developmental regulators via hijacking the plant ubiquitin receptor RPN10 independent of substrate ubiquitination [34]. Thus, the degradation of ABI4 may also not be dependent on ubiquitination entirely.…”

Section: Discussionmentioning

confidence: 70%

Hydrogen Sulfide-Linked Persulfidation Maintains Protein Stability of ABSCISIC ACID-INSENSITIVE 4 and Delays Seed Germination

Zhou

Zhang

Zhou

et al. 2022

IJMS

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Hydrogen sulfide (H2S) is an endogenous gaseous molecule that plays an important role in the plant life cycle. The multiple transcription factor ABSCISIC ACID INSENSITIVE 4 (ABI4) was precisely regulated to participate in the abscisic acid (ABA) mediated signaling cascade. However, the molecular mechanisms of how H2S regulates ABI4 protein level to control seed germination and seedling growth have remained elusive. In this study, we demonstrated that ABI4 controls the expression of L-CYSTEINE DESULFHYDRASE1 (DES1), a critical endogenous H2S-producing enzyme, and both ABI4 and DES1-produced H2S have inhibitory effects on seed germination. Furthermore, the ABI4 level decreased during seed germination while H2S triggered the enhancement of the persulfidation level of ABI4 and alleviated its degradation rate, which in turn inhibited seed germination and seedling establishment. Conversely, the mutation of ABI4 at Cys250 decreased ABI4 protein stability and facilitated seed germination. Moreover, ABI4 degradation is also regulated via the 26S proteasome pathway. Taken together, these findings suggest a molecular link between DES1 and ABI4 through the post-translational modifications of persulfidation during early seedling development.

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“…An important feature of phytoplasmas is their ability to modulate host plant development through effectors, which are small secreted proteins (Sugio et al, 2011b;Sugio and Hogenhout, 2012). To date, four phytoplasma effectors have been experimentally characterized, including SAP05 (Gamboa et al, 2019;Huang and Hogenhout, 2019;Huang et al, 2021), SAP11/SWP1 (Bai et al, 2009;Sugio et al, 2011a;Lu et al, 2014;Chang et al, 2018;Wang et al, 2018cWang et al, , 2018b, SAP54/PHYL1 (MacLean et al, 2011;Maejima et al, 2014;Orlovskis and Hogenhout, 2016), and TENGU (Hoshi et al, 2009;Sugawara et al, 2013;Minato et al, 2014). The expanded genome sequence availability allowed us to investigate the phylogenetic distribution of homologous effector genes among diverse phytoplasmas.…”

Section: Effector Genesmentioning

confidence: 99%

Comparative Genome Analysis of ‘Candidatus Phytoplasma luffae’ Reveals the Influential Roles of Potential Mobile Units in Phytoplasma Evolution

Huang

Cho

et al. 2021

Preprint

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Phytoplasmas are insect-transmitted plant pathogens that cause substantial losses in agriculture. In addition to economic impact, phytoplasmas induce distinct disease symptoms in infected plants, thus attracting attention for research on molecular plant-microbe interactions and plant developmental processes. Due to the difficulty of establishing an axenic culture of these bacteria, culture-independent genome characterization is a crucial tool for phytoplasma research. However, phytoplasma genomes have strong nucleotide composition biases and are repetitive, which make it challenging to produce complete assemblies. In this study, we utilized Illumina and Oxford Nanopore sequencing technologies to obtain the complete genome sequence of 'Candidatus Phytoplasma luffae' strain NCHU2019 that is associated with witches' broom disease of loofah (Luffa aegyptiaca) in Taiwan. The fully assembled circular chromosome is 769 kb in size and is the first representative genome sequence of group 16SrVIII phytoplasmas. Comparative analysis with other phytoplasmas revealed that NCHU2019 has an exceptionally repetitive genome, possessing a pair of 75 kb repeats and at least 13 potential mobile units (PMUs) that account for ~25% of its chromosome. This level of genome repetitiveness is exceptional for bacteria, particularly among obligate pathogens with reduced genomes. Our genus-level analysis of PMUs demonstrated that these phytoplasma-specific mobile genetic elements can be classified into three major types that differ in gene organization and phylogenetic distribution. Notably, PMU abundance explains nearly 80% of the variance in phytoplasma genome sizes, a finding that provides a quantitative estimate for the importance of PMUs in phytoplasma genome variability. Finally, our investigation found that in addition to horizontal gene transfer, PMUs also contribute to intra-genomic duplications of effector genes, which may provide redundancy for neofunctionalization or subfunctionalization. Taken together, this work improves the taxon sampling for phytoplasma genome research and provides novel information regarding the roles of mobile genetic elements in phytoplasma evolution.

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Parasitic modulation of host development by ubiquitin-independent protein degradation

Cited by 95 publications

References 75 publications

Accelerating Complete Phytoplasma Genome Assembly by Immunoprecipitation-Based Enrichment and MinION-Based DNA Sequencing for Comparative Analyses

Accelerating Complete Phytoplasma Genome Assembly by Immunoprecipitation-Based Enrichment and MinION-Based DNA Sequencing for Comparative Analyses

Hydrogen Sulfide-Linked Persulfidation Maintains Protein Stability of ABSCISIC ACID-INSENSITIVE 4 and Delays Seed Germination

Comparative Genome Analysis of ‘Candidatus Phytoplasma luffae’ Reveals the Influential Roles of Potential Mobile Units in Phytoplasma Evolution

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