Abstract Phytoplasmas are phloem‐restricted plant‐pathogenic bacteria transmitted by insects. They cause diseases in a wide range of host plants, resulting in significant economic and ecological losses worldwide. Research on phytoplasmas has a long history, with significant progress being made in the past 30 years. Notably, with the rapid development of phytoplasma research, scientists have identified the primary agents involved in phytoplasma transmission, established classification and detection systems for phytoplasmas, and 243 genomes have been sequenced and assembled completely or to draft quality. Multiple possible phytoplasma effectors have been investigated, elucidating the molecular mechanisms by which phytoplasmas manipulate their hosts. This review summarizes recent advances in phytoplasma research, including identification techniques, host range studies, whole‐ or draft‐genome sequencing, effector pathogenesis and disease control methods. Additionally, future research directions in the field of phytoplasma research are discussed.

Phytoplasma: A plant pathogen that cannot be ignored in agricultural production—Research progress and outlook

To perform its propagative and circulative cycle into its insect vector, the flavescence dorée phytoplasma invades different cell types. Clathrin-mediated endocytosis is used by a wide range of bacteria to infect eukaryote cells. Among the insect proteins interacting with the phytoplasma adhesin VmpA, we identified the adaptor protein complex AP-1 and AP-2 suggesting that phytoplasmas could enter the insect cells via clathrin-mediated endocytosis. By infection assays of insect cells in culture, we showed that phytoplasmas entry into Drosophila S2 cells was more efficient than infection of the Euva cell line developed from the insect vector Euscelidius variegatus. Chlorpromazine, cytochalasin D and knockdown of clathrin heavy chain (chc) gene expression using RNA interference inhibited entry of phytoplasmas into S2 cells. During invasion of S2 cells, phytoplasmas were observed very closed to recombinant GFP-labelled clathrin light chain. To verify the role of clathrin in the insect colonization by phytoplasmas, RNAi was performed via artificial feeding of chc dsRNA by the vector E. variegatus. This decreased the expression of chc gene in the midgut and heads of E. variegatus. The chc lower expression correlated to a decreased of midgut and salivary gland cells colonization after the insects had ingested phytoplasmas from infected plants. In conclusion, results indicate that clathrin is important for the FD phytoplasma to enter insect cells and colonize its insect vector. 

/pdf/flavescence-doree-phytoplasma-enters-insect-cells-by-a-3bsb2hx3.pdf

Flavescence dorée phytoplasma enters insect cells by a clathrin-mediated endocytosis allowing infection of its insect vector

Micropropagated Catharantus roseus plants infected with ‘Candidatus Phytoplasma asteris’ showed virescence symptoms, witches’ broom symptoms, or became asymptomatic after their planting in pots. Nine plants were grouped into three categories according to these symptoms, which were then employed for investigation. The phytoplasma concentration, as determined by qPCR, correlated well with the severity of symptoms. To reveal the changes in the small RNA profiles in these plants, small RNA high-throughput sequencing (HTS) was carried out. The bioinformatics comparison of the micro (mi) RNA and small interfering (si) RNA profiles of the symptomatic and asymptomatic plants showed changes, which could be correlated to some of the observed symptoms. These results complement previous studies on phytoplasmas and serve as a starting point for small RNA-omic studies in phytoplasma research.

/pdf/small-rna-profiling-of-aster-yellows-phytoplasma-infected-21x8adzw.pdf

Small RNA Profiling of Aster Yellows Phytoplasma-Infected Catharanthus roseus Plants Showing Different Symptoms

RNA silencing is a general strategy for eukaryotes including plants to resist pathogens, especially virus. In turn, virus have evolved RNA silencing suppressors (RSSs) to overcome RNA silencing in plants. In following researches, bacterial, oomycete, fungi have been found to involve in RSS besides virus. In 2021, we initially identified a novel RSS SWP16 from 37 secretory proteins encoded by phytoplasma. In this research, we analyzed the molecular and biological characters of SWP16 including bioinformatics analysis, subcellular localization, effect of SWP16 on plant innate immunity and phylogenetic analysis of SWP16. The results showed that SWP16 is a novel secretory protein which contains an α helix tertiary structure, 5 threonine (T) phosphorylation sites, 2 threonine (S) phosphorylation sites. Furthermore, a Leucine-rich repetitive structure (LRR) was harbored in the transmembrane domain of signal peptide of SWP16, furthermore, a putative secreting model of SWP16 was constructed. In addition, SWP16 localized in nucleus and cytomembrane. In this research, SWP16 was also found not to involve in HR-PCD processes of plant, so it suggested that SWP16 may specifically interfere RNA silencing in plant. The phylogenetic analysis demonstrated that SWP16 was highly conserved in evolution and shared high homology with a homology protein in onion yellows phytoplasma.

Biological characterization and evolution of a novel RNA silencing suppressor SWP16 from wheat blue dwarf (WBD) phytoplasma

Molecular mechanisms of plant manipulation by secreting effectors of phytoplasmas

Plants possess an innate immune system for defence against pathogens. In turn, pathogens have various strategies to overcome complex plant defences. Among diverse pathogens, phytoplasmas are associated with serious diseases in a range of species. RNA silencing serves as an efficient defence system against pathogens in eukaryotes but can be interrupted by RNA silencing suppressors (RSSs) encoded by pathogens. Currently, many RSSs have been identified in viruses, bacteria, oomycetes and fungi. Phytoplasmas are pathogens in several hundred plant species. In this research, 37 candidate effectors of wheat blue dwarf (WBD) phytoplasma were screened for presence of RSS. Agro-infiltration assay, yeast expression system, floral-dip method for constructing transgenic A. thaliana, Western blotting and RT-qPCR were used for identification of RNA silencing suppressors. SWP16 encoded by WBD phytoplasma was found to be a secretory protein that inhibited accumulation of GFP siRNA and led to the accumulation of GPF mRNA in systemic N. benthamiana 16c. Furthermore, in A. thaliana SWP16 inhibited production of miRNAs, which are components of RNA silencing. SWP16 also promoted infection of potato virus X. We conclude that SWP16 encoded by WBD phytoplasma was an RSS, suppressing systemic RNA silencing. This is the first evidence that a phytoplasma encodes an RSS and provides a theoretical basis for research on the interaction mechanisms between pathogens and plants.

Identification of RNA silencing suppressor encoded by wheat blue dwarf (WBD) phytoplasma

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Identification of RNA silencing suppressor encoded by wheat blue dwarf (WBD) phytoplasma