Next Article in Journal
Addressing Sexually Transmitted Infections Due to Neisseria gonorrhoeae in the Present and Future
Next Article in Special Issue
Divergence within the Taxon ‘Candidatus Phytoplasma asteris’ Confirmed by Comparative Genome Analysis of Carrot Strains
Previous Article in Journal
Advancements in Fermented Beverage Safety: Isolation and Application of Clavispora lusitaniae Cl-p for Ethyl Carbamate Degradation and Enhanced Flavor Profile
Previous Article in Special Issue
Risk Assessment for the Spread of Flavescence Dorée-Related Phytoplasmas from Alder to Grapevine by Alternative Insect Vectors in Germany
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 12
Issue 5
10.3390/microorganisms12050885
microorganisms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Paulownia Witches’ Broom Disease: A Comprehensive Review

by
Yajie Zhang
1,2,†,
Zesen Qiao
1,†,
Jidong Li
1,3,* and
Assunta Bertaccini
3,*
1
College of Forestry, Henan Agricultural University, Zhengzhou 450000, China
2
Henan Provincial Institute of Scientific and Technical Information, Zhengzhou 450003, China
3
Department of Agriculture and Food Science, Alma Mater Studiorum—University of Bologna, 40127 Bologna, Italy
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Microorganisms 2024, 12(5), 885; https://doi.org/10.3390/microorganisms12050885
Submission received: 2 April 2024 / Revised: 25 April 2024 / Accepted: 26 April 2024 / Published: 28 April 2024
(This article belongs to the Special Issue Phloem Localized Insect Transmitted Bacteria Associated with Plant Diseases)
Browse Figures
Review Reports Versions Notes

Abstract

:
Phytoplasmas are insect-transmitted bacterial pathogens associated with diseases in a wide range of host plants, resulting in significant economic and ecological losses. Perennial deciduous trees in the genus Paulownia are widely planted for wood harvesting and ornamental purposes. Paulownia witches’ broom (PaWB) disease, associated with a 16SrI-D subgroup phytoplasma, is a destructive disease of paulownia in East Asia. The PaWB phytoplasmas are mainly transmitted by insect vectors in the Pentatomidae (stink bugs), Miridae (mirid bugs) and Cicadellidae (leafhoppers) families. Diseased trees show typical symptoms, such as branch and shoot proliferation, which together are referred to as witches’ broom. The phytoplasma presence affects the physiological and anatomical structures of paulownia. Gene expression in paulownia responding to phytoplasma presence have been studied at the transcriptional, post-transcriptional, translational and post-translational levels by high throughput sequencing techniques. A PaWB pathogenic mechanism frame diagram on molecular level is summarized. Studies on the interactions among the phytoplasma, the insect vectors and the plant host, including the mechanisms underlying how paulownia effectors modify processes of gene expression, will lead to a deeper understanding of the pathogenic mechanisms and to the development of efficient control measures.

1. Introduction

Phytoplasmas are wall-less bacterial plant pathogens provisionally classified to the ‘Candidatus Phytoplasma’ genus [1,2]; they are mainly transmitted by insect vectors and inhabit the phloem of plants and the hemolymphs of insects. After colonization, phytoplasmas secrete effector proteins into cytoplasm of the host plant cells. These effectors interact with certain target proteins in the plant cell, manipulate several host metabolic pathways inducing a series of disease symptoms that includes witches’ broom (shoot proliferation), phyllody (leafy flower) and virescence, leaf yellowing and decline, stunted and little leaf, white leaf, purple top and other malformations. Some of the symptoms, such as witches’ broom and phyllody, increase the prevalence of short branches and small young leaves, enhancing attraction of insect vectors and thus benefit the spread of phytoplasmas [1,2].
The axenic culture of phytoplasmas is difficult to achieve; thus, the Koch postulates to confirm their role as pathogens are not yet fulfilled. Limited knowledge of their biological properties hindered their classification; therefore, phytoplasmas were classified using 16S rRNA gene sequences. Up to now, there are 36 published 16Sr phytoplasma groups and 49 ‘Ca. Phytoplasma’ species that infect more than 1000 plant species and cause significant economic losses [3,4].
The genus Paulownia, within the Paulowniaceae family, includes 17 fast growing, hard wood tree species. The most commonly cultivated species are Paulownia fortunei, P. catalpifolia, P. tomentosa and P. elongate [5,6]. The paulownias are mainly distributed in south-eastern Asia (especially China), where they were cultivated for over 2000 years for wood and ornamental purposes [6]. The genus name Paulownia Siebold & Zucc was recorded by German botanist Philipp Franz von Siebold, to honor Anna Pavlovna Romanova, grand duchess of Russia and queen of the Netherlands, who sponsored Philipp’s expedition to Japan. Therefore, the paulownia tree is also known as the princess tree and the royal tree [7], while its Chinese name is 泡桐 (pao tong). Nowadays, paulownia trees are widely planted across Asia, North America, Europe and Australia for commercial and decorative purposes [6].
Paulownia witches’ broom (PaWB) (Figure 1) is the most destructive disease affecting paulownia and causes serious economic losses [8]. It is associated with the presence of PaWB phytoplasmas [9] and it has been studied for more than 100 years; however, the pathogenic mechanisms, especially the molecular mechanisms underlying the disease symptoms, are still not clear. Efficient and economically feasible prevention and control methods for PaWB have still not been achieved. This review summarizes both the past of PaWB disease research, and the up-to-date knowledge about research on the pathogenic mechanisms of the associated phytoplasma at the molecular level. A PaWB pathogenic mechanism frame diagram on molecular level is summarized in Figure 2, and future and prospective research directions are put forward.

2. Historical Background

PaWB was one of the first phytoplasma diseases in the world to be studied. According to Kawakami’s report in 1902, PaWB disease was first observed in 1880, in Kumamoto, Japan [10]. In China, the Japanese phytopathologist, Ichiro Miyake, serving as a professor in the Imperial University of Peking, now China Agricultural University, reported “paulownia anthrax disease”, with witches’ broom symptoms, in Liaoning province in 1910 [11]. An occurrence of PaWB disease was also reported in Korea [12].
Since PaWB could be transmitted by grafting, it was first believed to be a viral disease. In 1967, Doi et al. discovered mycoplasma-like structures in ultrathin sections of the phloem of plants affected by paulownia witches’ broom, as well as mulberry dwarf and aster yellows [13]. The term mycoplasma-like organisms (MLOs) was used to refer to the agents associated with these diseases. In 1992, the name “phytoplasma” was adopted by the Phytoplasma Working Team at the 9th Congress of International Organization of Mycoplasmology to collectively denote MLOs [14]. In 2004, these non-helical, cell wall-less bacteria were placed within the novel provisional genus ‘Candidatus Phytoplasma’ [15]. The PaWB phytoplasma is a strain of ‘Candidatus Phytoplasma asteris’, belonging to ribosomal subgroup 16SrI-D [3,4,9].

3. The Paulownia Witches’ Broom Phytoplasma

Although the cultivation of PaWB phytoplasma in an artificial medium has still not been achieved, grafting, DAPI (4′,6-diamidino-2-phenylindole) staining, TEM (transmission electron microscopy) observation and PCR (polymerase chain reaction) detection, have provided sufficient evidence that PaWB phytoplasma is the bacterial pathogen associated with the disease. The PaWB phytoplasma occur as round or elliptical particles with a diameter of 200–820 nm, localized in the sieve tubes of plant phloem when observed with an electron microscope [16].
In the paulownia cultivation areas in China, phytoplasmas in the 16SrI-D subgroup were found associated with other plants, such as Japanese maple (Acer palmatum) [17], Kerria japonica [18], peach (Prunus persica) [19], rose balsam (Impatiens balsamina) [20], rose (Rosa rugosa) [21] and R. xanthina [22], Syringa oblata and S. reticulata [23] and shiny leaf yellow horn (Xanthoceras sorbifolium) [24]. Most of them occur nearby or close to the PaWB-diseased paulownia trees.
Paulownias are deciduous tree species in temperate regions. Thus, the distribution of phytoplasmas in paulownia trees varies among different seasons with the temperature [25]. In the northern hemisphere, the phytoplasma concentration in branches and leaves peaks in July and August, when temperatures are high, and the tree is growing vigorously. In the winter, the phytoplasma levels in branches and leaves are very low but still detectable with nested PCR. Changes in phytoplasma content in roots are not as dramatic as those in branches and leaves [26,27].
Genetic diversity exists in the PaWB phytoplasma populations. A population structure study on 142 PaWB phytoplasma strains from 18 provinces in China indicated comparatively high genetic diversity. The phylogenetic analysis was performed through the sequence analysis of 10 housekeeping genes, namely 16S rRNA, rp, fusA, secY, tuf, secA, dnaK, rpoB, pyrG, gyrB and ipt. The results showed that the 142 PaWB phytoplasma strains clustered into two main lineages with obvious geographical differentiation [28].

4. Transmission of PaWB Phytoplasmas

Phytoplasmas are transmitted by phloem-feeding insect vectors, mainly leafhoppers, planthoppers and psyllids. Transmission experiments have confirmed that stink bugs (such as Halyomorpha mista in Japan [29], H. halys, and H. picus in China, [30]), mirid bugs (such as Cyrtopeltis tenuis in Korea [31]) and leafhoppers (such as Empoasca sp. in Korea [32] and Hishimonoides chinensis in China [33]) are insect vectors of PaWB. In addition to transfer by insect vectors, PaWB phytoplasma can also be transmitted by root cutting, the most popular vegetative propagation material [29]. There are no reports on PaWB phytoplasma transmission by seed [34].

5. Symptomatology of PaWB Disease

The most characteristic symptom of PaWB disease is excessive shoot proliferation. Axillary buds break without limit, and shoots and branches grow without restriction (Figure 1). This symptom is commonly called witches’ broom, as it resembles a broom made from bundled twigs that a witch might use to fly, and “Tengu-su” (Tengu’s nest) in Japan, as the numerous short branches resemble the nest of “Tengu”, a mythical, long-nosed goblin who lives in the mountain and flies through the sky [35].
Diseased paulownia trees, regardless the species or geographical area, show the same symptoms. Leaves are smaller and thinner than healthy leaves, and their color fades to yellow. Malformed leaves are often observed on the diseased shoots. The surfaces of diseased leaves are uneven, and the hairs on the underside of the leaves grow sparsely. Reproduction of diseased trees is affected, as phyllody (leafy flower) also occurs. The stigma elongates as a twig, while the sepal, petal and stamen turn into small leaves. Roots of the diseased trees are weak and brownish, easily decay and have little regeneration vigor [10,36].
Diseased paulownias begin to show witches’ broom in late spring. The symptoms are not restricted to a specific part of a tree. Shoot proliferation occurs on one or a few branches, then spreads to the adjacent branches until the entire canopy becomes affected (Figure 1). Leaves on the lower part of the diseased shoots fall in late summer or early autumn, while leaves on the upper part of diseased branches remain attached. Axillary buds continue to sprout in late autumn or even in winter. Diseased trees die within a few years after the witches’ broom symptom first appears [10,36].

6. Physiological and Anatomic Responses to Phytoplasma Infection

The presence of phytoplasmas alters many physiological indicators in paulownia, such as metabolite content levels and related enzyme activity. Radioisotope tracer assays indicated that the phosphorus/potassium (P/K) ratio, and the total phenolic and chlorogenic acid contents in diseased trees are lower than in healthy ones [37,38]. The protein and vitamin C contents are higher in diseased trees [39,40].
Several indicators of plant stress and disease response are altered in diseased plants. Peroxidase (POD) enzyme activity and malondialdehyde (MDA) contents were higher in diseased P. fortune leaves, while superoxide dismutase (SOD) enzyme activity was higher in the healthy leaves [41]. The POD isozyme bands in different organs of diseased P. tomentosa show varying degrees of reduction compared to the corresponding organs of healthy trees. Furthermore, the POD isozyme bands in PaWB-diseased trees varied in different seasons [42,43].
Phytoplasma infection can also change anatomical structures within paulownia trees. The thickness of the cambium and the diameter of the secondary xylem vessels are reduced in diseased branches. The mesophyll palisade tissue in leaves becomes slim. The amount of hair on the lower page of infected leaves diminishes [44]. The infected small leaves in the diseased trees have blades that are less thick, with reduced and spongy palisade tissues. The length of wood fibers decreases in diseased trees, while the fiber width and cell cavity increase [45].

7. Changes in Gene Expression in Phytoplasma-Infected Paulownia

Analyses using simple sequence repeat (SSR) [46,47] and amplified fragment length polymorphism (AFLP) [48,49] molecular markers indicated that infection with phytoplasma did not cause changes in paulownia DNA sequences. The gene expression variation after phytoplasma infection seems to be the key to the induction of disease symptom. The mechanisms underlying gene expression differentiation in phytoplasma-infected paulownia have been studied at the transcriptional, post-transcriptional and translational levels (Table 1).

7.1. Transcriptional Responses

The DNA methylation level within genomes of diseased paulownia seedlings is significantly decreased compared to healthy ones [50]. Treatment with tetracycline can recover health and increase the DNA methylation level of diseased seedlings. Treatment with the DNA methylation agent methyl methane sulfonate (MMS) can also recover the health of diseased in vitro plantlets and increase their DNA methylation level [46]. These clues led to investigations of gene expression patterns, using techniques such as de novo transcriptome sequencing and RT-qPCR (retrotranscripted quantitative PCR) on healthy, PaWB-diseased and MMS-treated diseased paulownia plants. Many differentially expressed genes (DEGs) among these samples were identified. Studies using the gene ortholog (GO) functional and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway databases indicated that these DEGs are involved in various pathways, including phytohormone biosynthesis, photosynthesis and plant–pathogen interaction [51,52,53,54,55,56,57,58].
Third generation sequencing of full-length transcriptomes has also been performed on paulownia, to gauge gene expression responses to phytoplasmas. Combined with metabolome data, a model of the early defense response to PaWB disease was constructed [59].
Table 1. High-throughput analyses on genomic and gene expression responses to PaWB phytoplasma.
Table 1. High-throughput analyses on genomic and gene expression responses to PaWB phytoplasma.
Plant MaterialAnalysis MethodsPrimary Analysis ResultsCorresponding PathwaysKey Corresponding GenesReferences
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.AFLP, MSAP and RT-qPCR.81 methylated fragments and 6 DEGs. [48]
P. tomentosa, healthy, diseased and MMS-treated diseased in vitro plantlets.AFLP, MSAP and RT-qPCR.72 methylated fragments and 6 DEGs. [49]
Paulownia spp., healthy and diseased field trees, in vitro plantlets.Transcriptome sequencing and RT-qPCR.1271 DEGs in field trees, 1206 DEGs in in vitro plantlets and 19 common KEGG pathways.Cytokinin biosynthesis, photosynthesis, cell wall biosynthesis and degradation.Isopentenyl diphosphate isomerase and isopentenyl-transferase.[51]
P. tomentosa × P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.Transcriptome sequencing and RT-qPCR.74 significant DEGs and 16 KOGs categories.General function, posttranslational modification and protein turnover. [52]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.Transcriptome sequencing and RT-qPCR.1309 DEGs and 83 KEGG pathways.Plant–pathogen interaction, circadian rhythm, hormone-related. [53]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.Transcriptome sequencing and RT-qPCR.618 DEGs and 82 KEGG pathways.Phenylpropanoid metabolism, hormone biosynthesis and signaling, defense and/or pathogenesis and signal transduction. [54]
P. tomentosa, healthy, diseased and MMS-treated diseased in vitro plantlets.Transcriptome sequencing and RT-qPCR.2540 DEGs and 119 KEGG pathways.Folate and fatty acid synthesis and plant hormone signal transduction. [55]
P. tomentosa, P. fortunei and P. tomentosa × P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.Transcriptome sequencing and RT-qPCR.74 DEGs and 12 KEGG pathways.Phytohormone and alternative splicing. [56]
P. tomentosa, healthy, diseased and MMS-treated diseased in vitro plantlets.Transcriptome, miRNA and degradome sequencing and RT-qPCR.902 DEGs, 24 PaWB-related DERs and19 target genes among the DEGs.Morphological changes, plant defense and plant hormones.miR156g, miR166c and miR403.[57]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.Transcriptome, miRNA and degradome sequencing and RT-qPCR.756 DEGs, 67 PaWB-related DERs and 635 target genes among the DEGs. ARF, WRKY, NAC, MYB and SOD.[58]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.Full-length transcriptome sequencing, LC-ESI-MS/MS metabolism and RT-qPCR.1561 full length transcripts and 645 metabolites related to PaWB. SA-binding protein 2, ferulic acid and ethylene-responsive transcription factor RAP2–7 isoform X2.[59]
P. tomentosa × P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.miRNA and degradome sequencing and RT-qPCR.33 PaWB-related DERs (13 conserved and 20 novel) and 166 DER target genes.Plant–pathogen interactions and plant hormone signal transduction, metabolic features. [60]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.miRNA and degradome sequencing and RT-qPCR.37 PaWB-related DERs (14 conserved and 24 novel) and 147 DER target genesTranscription, stress response and nitrogen metabolismmiR159-3p, miR169a/b, miR169l, miR171a/b/c/d, miR1-3p, miR17b, miR30-3p and miR32-3p.[61]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.miRNA and degradome sequencing and RT-qPCR.38 PaWB-related DERs (17 conserved and 20 novel) and 166 target genes of the DERs. miR160c, miR167, miR171, miR397, miR398a and miR399a/b.[62]
P. tomentosa, P. fortunei and P. tomentosa × P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.miRNA and degradome sequencing and RT-qPCR.76 common DERs (35 miRNA families) from three paulownia species and 196 target genes.Photosynthesis, plant hormone, plant defense, energy metabolism and material metabolic.miR156.[63]
P. tomentosa, healthy, diseased and rifampin-treated diseased in vitro plantlets.High throughput RNA sequencing and RT-qPCR.1063 PaWB-related mRNAs, 110 PaWB-related lnc RNAs and 12 PaWB-related target genes. [64]
P. fortunei, healthy, and diseased in vitro plantlets.High throughput RNA sequencing.2725 lncRNAs and 748 DELs.Lignin biosynthesis, plant–pathogen interaction and plant hormone signal transduction. [65]
P. tomentosa, healthy, diseased and MMS-treated diseased in vitro plantlets.High throughput RNA sequencing and RT-qPCR.3689 lncRNAs, 112 DELs and 51 alternatively spliced target genes.Reactive oxygen species-induced hypersensitive response and effector-triggered immunity. [66]
P. fortunei, healthy and diseased in vitro plantlets.High throughput RNA sequencing.229 lncRNAs, 65 circRNAs and 65 miRNAs, differentially expressed.Phytohormone biosynthesis, signal transduction, protein processing, amino acid metabolism, chloroplast and defense response. [67]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.m6A transcriptome sequencing and m6A MeRIP RT-PCR.315 differential methylated genes. CLV2, STM, F-box and MSH5.[68]
P. tomentosa, healthy, diseased and MMS-treated diseased in vitro plantlets.iTRAQ proteome sequencing and RT-qPCR2051 proteins and 43 PaWB-related DAPs.Photosynthesis, expression of dwarf symptom, energy production and cell signal pathways. [69]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.iTRAQ proteome sequencing and RT-qPCR2358 proteins and 36 PaWB-related DAPs.Carbohydrate and energy metabolism, protein synthesis and degradation and stress resistance. [70]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.iTRAQ proteome sequencing and RT-qPCR.2969 proteins and 27 PaWB-related DAPs.Photosynthesis-related, energy-related and ribosome-related. [71]
P. tomentosa, healthy, diseased, MMS-treated healthy and diseased in vitro plantlets.Quantitative mass spectrometry proteome, acetylome and succinylome.8963 proteins, 546 PaWB-related acetylated proteins and 5 PaWB-related succinylated proteins.Protochlorophyllide reductase, RuBisCO and chlorophyll and starch biosynthesis. [72]
P. fortunei, healthy and diseased in vitro plantlets.Hi-C sequencing
RNA-seq.		477 and 510 specific TAD boundaries, 2304 and 3540 specific chromatin loops in healthy and diseased samples and 694 DEGs in common loops. 11 PaWB-closely related genes.[73]
P. fortunei, healthy and diseased in vitro plantlets.ChIP-seq and ChIP-qPCR.1821, 1159 and 2727 DMGs marked by H3K4me3, H3K36me3 or H3K9ac and 141 co-modified DMGs.Metabolic pathways, biosynthesis of secondary metabolites, phenylpropanoid biosynthesis, plant–pathogen interaction and plant hormone signal transduction. [74]
P. fortunei, healthy, diseased and MMS-treated diseased in vitro plantlets.Chip-seq and RNA-seq.365, 2244 and 752 PaWB-associated genes with H3K4me3, H3K36me3 and H3K9ac methylation.Plant–pathogen interaction, plant hormone signal transduction and starch and sucrose metabolism [75]
P. fortunei, healthy and diseased in vitro plantlets.Bisulfite and transcriptome sequencing, bisulfite-PCR and RT-qPCR.422,662 DMRs, 27,871 DMR-associated DEGs and 436 genes verified by RNA-seq.Plant hormone signal transduction, carbon metabolism and starch and sucrose metabolism.TPR1 and R2R3-MYB[76]
DERs, differentially expressed RNAs; MS, mass spectrometric; LC-ESI-MS, liquid chromatography electrospray ionization MS; RNA, ribonucleic acid; mRNAs, messenger RNAs; lncRNAs, long noncoding RNAs; DELs, differentially expressed RNAs; circRNAs; circular RNAs; m6A, N6-methyladenosine; MeRIP, methylated RNA immunoprecipitation; CLV2, CLAVATA2; STM, SHOOT MERISTEMLESS; MSH5, MutS protein homologs 5; iTRAQ, isobaric tags for relative and absolute quantification; DAPs, differentially abundant proteins; RuBisCO, ribulose bisphosphate carboxylase oxygenase; Hi-C, high-throughput chromosome conformation capture; ChIP-seq, chromatin immunoprecipitation sequencing; ChiP-qPCR, chromatin immunoprecipitation quantitative PCR; TADs, topologically associated domains; DMGs, differentially marked genes; DMRs, differentially methylated RNAs; TPR1, TOPLESS RELATED 1.
Mining the paulownia genome data identified some transcription factor (TF) and functional gene families, such as ARF [77], Aux/IAA [78], BTB [79], bZIP [80], CaM/CML [81], GRAS [82], MADS [83], NCED [84], NLR [85], PP2C [86], SERK [87], SPL [88], TCP [89], UBC E2 [90], and WPR [91], that could be affected by phytoplasma colonization. Expression pattern analyses of transcriptome data and using RT-qPCR further showed that some of these gene family members were differentially expressed among healthy, diseased and MMS-treated diseased in vitro paulownia plantlets, indicating that they may be related to the presence of PaWB phytoplasmas (Table 2).

7.2. Post Transcript Response

7.2.1. Noncoding Ribonucleic Acids

Noncoding RNAs, such as microRNAs (miRNAs), long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs), play important roles in the post-transcriptional regulation of cellular activities. MicroRNAs are small, single-strand, non-coding RNA molecules of 21 to 23 nucleotides. MicroRNAs bind to complementary mRNA sequences, leading to the cleavage or destabilization of mRNA, which negatively impacts the expression of the target gene [92]. LncRNAs are non-coding transcripts of more than 200 nucleotides, while circRNAs are single-strand RNA molecules that form a covalently closed continuous loop. Both are believed to be involved in gene expression regulation, although their functions are not yet clearly defined [93].
High-throughput sequencing and degradome analyses have been performed on healthy, diseased and MMS-treated diseased paulownia in vitro plantlets to reveal the functions of noncoding RNAs involved in PaWB. Some differentially expressed miRNAs (DERs) [57,58,60,61,62,63], lncRNAs (DELs) [64,65,66,67] and circRNAs [67], as well as target genes of the DERs/DELs, have been identified and likely play important roles in responding to PaWB infection. A competing endogenous RNA (ceRNA) network that includes these differentially expressed miRNAs, circRNAs, lncRNAs and mRNAs has been constructed [67].

7.2.2. Splice Variants

RNA molecules can undergo alternative splicing (AS) to generate multiple mRNA transcript variants from a single gene. AS increases transcriptome plasticity and proteome diversity and is an important post-transcriptional regulatory mechanism. Analysis using high-throughput transcriptome sequencing has identified many alternative splicing variants of paulownia mRNAs [56,58,59,65,66]. The AS frequency in healthy paulownia is higher than in PaWB-diseased samples. Some AS events occur for genes that are differentially expressed between healthy and PaWB-diseased paulownia, implying that splice variants may be related to the paulownia response to PaWB.

7.2.3. Messenger RNA Modification (Epitranscriptome)

Messenger RNA (mRNA) modification is an essential and widespread molecular mechanism underlying key plant developmental process, including embryo development, shoot stem cell fate, floral transition, trichome morphogenesis, leaf initiation and root development [94]. The addition of an N6-methyladenosine (m6A) is the most common post-transcriptional modification of mRNA. An m6A modification is involved in regulating mRNA expression, translation efficiency, alternative splicing and mRNA degradation. The m6A transcriptome was sequenced for PaWB-diseased and PaWB-recovered (MMS-treated diseased, 16S rRNA gene-nested PCR-negative) P. fortunei plantlets grown in vitro [68]. The results indicated that MMS treatment lowered the m6A modification degree in PaWB-recovered paulownia, compared to diseased plantlets. When combined with RNA-seq data, 315 differentially methylated genes (DMGs) were screened from DEGs. Functional enrichment analysis revealed that CLV2 and STM, related to the maintenance of stem cells in shoot apical meristem, were involved in the PaWB–plant interaction. Moreover, alternative splicing was found to be associated with m6A modification in F-box and MSH5 genes of MMS-treated diseased plantlets [68].

7.3. Translational and Post-Translational Response

7.3.1. Proteomic Analysis

Proteomic analysis, using isobaric tags for relative and absolute quantification (iTRAQ), can provide accurate, efficient and high-coverage protein quantification. With iTRAQ proteome analysis, differentially abundant proteins (DAPs) among healthy, diseased and MMS-treated diseased paulownia in vitro plantlets were identified. Functional analysis using GO, COG and KEGG databases revealed that proteins related to photosynthesis, energy metabolism and cell signal pathways were most involved in the response of paulownia to phytoplasmas [69,70,71].
The correlation between proteome and transcriptome data was poor among the healthy, diseased and MMS-treated diseased paulownia. The number of DAPs was much fewer than the number of DEGs. This suggests that the differences in transcript levels may not be carried through to changes in protein levels. This may be due to the transcriptional/post-transcriptional regulation, translational/post-translational regulation, protein modification or protein–protein interactions [69,70].

7.3.2. Lysine Acetylation and Succinylation

Lysine acetylation and succinylation are post-translational protein modifications that affect protein function and enzyme activity modulating the cellular metabolic status. Proteome, acetylome and succinylome analyses using quantitative mass spectrometry were performed on healthy, diseased, MMS-treated healthy and diseased P. tomentosa plantlets grown in vitro. This study revealed that 276 proteins, 546 acetylated proteins and 5 succinylated proteins were regulated, in response to phytoplasma infection. Acetylation of specific sites in protochlorophyllide reductase and RuBisCO are known to modify their activities. The modification of these proteins correlates with the decreased photosynthetic activity and starch accumulation in PaWB-diseased plantlets [72].

7.4. Genome Accessibility

7.4.1. Three-Dimensional Chromatin Structure

The 3-D chromatin conformation in the cell nucleus is closely related to gene expression and epigenetic regulation. High-throughput chromosome conformation capture (Hi-C) sequencing was used to profile the genome-wide chromatin conformation of healthy and PaWB-diseased P. fortunei. Phytoplasma infection altered the main structural characteristics of active and inactive chromosome regions (also known as A/B compartments), topologically associated domains and chromatin loops in paulownia plants [73].
Chromatin immunoprecipitation (ChIP) sequencing and RNA sequencing further showed that the infection with phytoplasmas changed the chromatin structure and transcriptional activity. The modification levels of three histones (H3K4me3/K9ac/K36me3) increased in diseased paulownia. Eleven genes associated with histone marks and located at specific topologically associated domain boundaries, A/B compartment switching and specific loops, were considered to be closely related to the paulownia–phytoplasma interaction [73].

7.4.2. Histone Methylation and Acetylation

Histone methylation and acetylation can influence genome accessibility, at levels ranging from local nucleosome dynamics to the folding of higher chromatin structure. Both methylation and acetylation promote open chromatin conformation and positively influence the genome accessibility [95]. Chromatin immunoprecipitation sequencing (ChIP-seq) was used to profile three histone marks, the methylation of histone H3 at lysine 4 (H3K4me3), the methylation of histone H3 at lysine 36 (H3K36me3) and the acetylation of histone H3 at lysine 9 (H3K9ac), among healthy, diseased and MMS-treated diseased P. fortunei plantlets grown in vitro [74,75]. The number of histone modification regions was higher in diseased paulownia than in healthy plants [74]. The combination of RNA-seq data and ChIP-qPCR revealed that histone modification positively activated gene expression. DEGs with differential histone modification profiles were mainly involved in calcium ion signal transduction, abscissic acid signal transduction and ethylene biosynthesis [75].

7.4.3. DNA Methylation

DNA methylation participates in various nuclear processes such as gene expression, DNA repair and recombination. Various studies have indicated that DNA methylation at gene boundaries contributes to a differential gene expression in response to pathogens [95]. Methylation-sensitive amplification polymorphism (MSAP) analysis revealed that the DNA methylation level of healthy plantlets is higher than the PaWB-diseased ones. Treatment with MMS increases DNA methylation levels and induces recovery from PaWB in the plantlets, restoring a healthy morphology. A few genes related to PaWB were discovered through sequencing the MSAP fragments and validated using RT-qPCR [48,49].
A DNA cytosine methylation map was constructed using data from whole genome bisulfite sequencing on healthy and PaWB-diseased P. fortunei in vitro plantlets. A total of 422,662 differentially methylated regions (DMRs) were identified. The combination of DNA methylation and transcriptome analyses identified 436 genes that differed in both methylation and transcript levels between healthy and diseased plantlets. Bisulfite-PCR and RT-qPCR validation of the DMR-associated genes suggest that DNA methylation has a repressive effect on gene expression. Two genes, TPR1 and R2R3-MYB, were proposed to be closely related to PaWB [76].

8. Genome and Effectors of Paulownia Witches’ Broom Phytoplasma

8.1. Paulownia Witches’ Broom Phytoplasma Genome

The complete genome of PaWB phytoplasma comprises 891,641 bp on one circular chromosome with a G + C content of 27.4%. This genome contains 1147 open reading frames, and it is predicted to encode two operons for rRNA genes, as well as 32 tRNA genes. Four potential mobile units (PMUs), ranging from 20 kb to 41 kb, were also identified [8]. Similar with the genome of onion yellows phytoplasma, the PaWB phytoplasma genome carries the genes encoding complete pathways for the metabolism of glycerophospholipid, glycolysis, pyrimidine and folate. One or more of these genes may be absent in the genome of six other phytoplasmas, according to whole genome comparative analysis [8].

8.2. Effectors

Seventy-three virulence effectors were predicted in the PaWB phytoplasma genome through analysis using four different bioinformatic tools [8]. The genes for forty PaWB effectors were transcribed in the apical buds of phytoplasma-infected paulownia. The expression of eleven of these effector genes was downregulated after 5 days of treatment with MMS and rifampicin and was undetectable after 20 days of treatment. One of the 11 effectors is an ortholog of the phytoplasma effector SAP54. Expression of SAP54PaWB in Populus trichocarpa results in axillary secondary branches along the stem, similar with the formation of witches’ broom symptom. SAP54PaWB interacted with PfSPLa, a member of the Squamosa-promoter binding protein-like (SPL) transcription factor family. The PfSPLa can interact with polyubiquitin and the 26S proteasome non-ATPase regulatory subunit 3 (PfRPN3). This suggests that SAP54PaWB promotes the degradation of PfSPLa in a ubiquitin/26S proteasome-dependent manner to induce shoot proliferation symptoms [8].
A frame diagram of the PaWB molecular pathogenic mechanism is summarized in Figure 2. The genetic information will flow according to DNA to RNA, then to protein. During this progression, epigenetic modifications also influence gene expression at various levels. Phytoplasmas multiply in the sieve cells of the phloem, secrete effector proteins into the neighbor tissue cells and interact with target proteins such as the SPL transcription factors, further influencing the transcription process. These regulation modifications result in normal or PaWB disease morphology.

9. Changes in the Microbiome in Response to Phytoplasma Infection

The plant endophytic microbes have a significant effect on plant nutrient acquisition, abiotic stress tolerance and protection against pathogens [96]. Phytoplasmas are part of the endophyte microbial community and are involved in the symbiotic interaction network. The effect of PaWB phytoplasma infection on the fungal and bacteria communities of paulownia were analyzed by 16S and ITS gene sequencing. The results showed that the abundance and diversity of endophytic fungal species is lower, but the bacterial diversity is higher in the diseased branches and leaves compared to healthy samples. The PaWB phytoplasma infection alters the structure, components and function of the paulownia endophytic microbial community. At the genus level, the abundance of all bacterial genera decreased in the diseased leaf samples except for the ‘Ca. Phytoplasma’, including some beneficial bacteria genera such as Bacillus, Pseudomonas, Novosphingobium, Methylobacterium and Sphingomonas [97,98].

10. Paulownia Witches’ Broom Control

10.1. Resistance of Paulownia to Phytoplasmas

Resistance to PaWB phytoplasma varies among the paulownia populations. A seven-year continuous observation on different paulownia species and hybrids showed that P. fortunei, P. kawakamii and P. tomentosa are slightly susceptible, each with a disease incidence less than 40% and a disease index lower than 0.15. P. photeinophylla, P. catalpifolia and P. australis are highly susceptible with disease incidences of, or higher than, 60% and disease indices higher than 0.3, while P. elongata and P. fargesii are moderately susceptible. Among 12 hybrids, P. fargesii × P. fortunei has the lowest disease incidence (26.7%) and disease index (0.08) [99]. Another observational study on different paulownia species selected one resistant type, P. tomentosa var. tsinlingensis, which has long and thick leaf hairs that have a long stalk and either a dendritic shape, forked shape, single branch shape or glandular shape with giant cells. All the leaf hairs are sticky, making it difficult for insect vectors to feed on the leaves of this paulownia accession [100].
There have been several successful attempts to induce resistance to PaWB in paulownia. In one study, the selection of disease-free seedlings after grafting with PaWB-diseased materials yielded a paulownia plantation with zero PaWB occurrence [101]. Grafting with diseased material increased the activities of POD, PPO (polyphenol oxidase) and PAL (phenylalanine ammonia-lyase) enzymes in paulownia seedlings and young trees, and thus inducing resistance to PaWB [102]. Resistance to PaWB could also occur through mutations induced by cobalt 60 radiation treatment [103].

10.2. Chemical Treatment

Phytoplasmas are sensitive to the antibiotic tetracycline [104]. Treatment with tetracycline, oxytetracycline or rifampicin, by soil drenching and trunk injection, can suppress PaWB symptoms. However, the symptoms may reoccur after the antibiotic treatments are suspended [36,105]. Tetracycline treatment can also be used to recover PaWB diseased plantlets grown in vitro to normal morphology [50]. The DNA methylation agent methyl methanesulfonate (MMS) can also return diseased in vitro plantlets to asymptomatic status, and with no detectable phytoplasma 16Sr RNA gene by nested PCR assay [46].

10.3. Field Management

Other management practices include disease-free seedling propagation, insect vector control by pesticides and removal of heavily diseased trees [36]. Treatment of root cuttings with hot water is an effective way to propagate disease-free seedlings. The most efficient treatment conditions are a hot water bath at 46 °C for 15 min [106]. One important cultural practice is the removal of the diseased branches by pruning before leaf fall in the autumn, which prevents phytoplasmas’ movements towards the roots with sap flow, which can reduce symptoms in the next year. On the contrary, the removal of diseased shoots in the spring will make things worse [107]. Thus far, the effective management of PaWB disease on the large scale is still insufficient.

11. Perspectives

Paulownia are perennial trees cultivated for wood and ornamental purposes [7]. Unlike other cereal or horticultural crops threatened by phytoplasma diseases [108], there is relatively little input into infected paulownia management. Outside of the necessary irrigation and fertilization when planting, other management measures are rarely used on paulownia plantations. Thus, the paulownia forest community structure is more complex than more uniform farmlands, and the biodiversity is more abundant. As an insect-transmitted disease, it is necessary to understand the interactions among plant hosts, phytoplasmas and insect vectors, especially the feeding behavior of the insect vectors to develop effective control strategies. More efforts should be put into this research area.
Many high-throughput sequencing studies conducted on PaWB provide massive data information for phytoplasma research. The amount of data for paulownia sequencing has reached the terabyte (TB) level, the largest in any phytoplasma-related disease research. These data can be used to shed light also on other phytoplasma disease research. However, the massive amounts of sequencing data can only provide information from a statistical perspective and must rely on bioinformatics analysis tools and logical study design for elaboration. The pathogenic mechanisms underlying molecular alterations discovered from high-throughput data should be verified in detail through biological experimentation. Understanding the mechanisms by which paulownia gene expression responds to phytoplasma effectors is of paramount importance.
The phytoplasma effector SAP54 and homologous have been reported to interact and degrade MADS domain proteins, inducing phyllody symptoms. In the paulownia phytoplasma, the effector SAP54PaWB is verified to interact and degrade the SPL transcription factor protein PfSPLa. The PfSPLa was further annotated as PfSPL4, and it was proven to interact with the promoter region of PfTCPa gene [88]. TCP transcript factors play a key role in plant growth regulation and have been reported as targets of phytoplasma effector SAP11 [109], while SPLs are targets of SAP05 [110]. Further research on the downstream influence of SAP54PaWB–SPL interaction may reveal novel pathogenic mechanisms of the effectors of this phytoplasma and further help in the clarification of pathogenicity mechanisms in paulownia.

Author Contributions

Conceptualization, J.L. and A.B.; literature references searching, Y.Z. and Z.Q.; writing—original draft preparation, Y.Z., Z.Q. and J.L.; writing—review and editing, J.L. and A.B.; funding acquisition, J.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Natural Science Foundation of Henan, grant number 232300420007; and China Scholarship Council, grant number 202209160001.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

We thank Anita K. Snyder for help in correcting the English of the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Bertaccini, A. Plants and phytoplasmas: When bacteria modify plants. Plants 2022, 11, 1425. [Google Scholar] [CrossRef]
  2. Wang, R.; Bai, B.; Li, D.; Wang, J.; Huang, W.; Wu, Y.; Zhao, L. Phytoplasma: A plant pathogen that cannot be ignored in agricultural production—Research progress and outlook. Mol. Plant Pathol. 2024, 25, e13437. [Google Scholar] [CrossRef]
  3. Bertaccini, A.; Arocha-Rosete, Y.; Contaldo, N.; Duduk, B.; Fiore, N.; Montano, H.G.; Kube, M.; Kuo, C.-H.; Martini, M.; Oshima, K.; et al. Revision of the ‘Candidatus Phytoplasma’ species description guidelines. Int. J. Syst. Evol. Microbiol. 2022, 72, 005353. [Google Scholar] [CrossRef] [PubMed]
  4. Wei, W.; Zhao, Y. Phytoplasma taxonomy: Nomenclature, classification, and identification. Biology 2022, 11, 1119. [Google Scholar] [CrossRef]
  5. Dżugan, M.; Miłek, M.; Grabek-Lejko, D.; Hęclik, J.; Jacek, B.; Litwińczuk, W. Antioxidant activity, polyphenolic profiles and antibacterial properties of leaf extract of various Paulownia spp. clones. Agronomy 2021, 11, 2001. [Google Scholar] [CrossRef]
  6. Slawinska, N.; Zajac, J.; Olas, B. Paulownia organs as interesting new sources of bioactive compounds. Int. J. Mol. Sci. 2023, 24, 1676. [Google Scholar] [CrossRef]
  7. Jakubowski, M. Cultivation potential and uses of paulownia wood: A review. Forests 2022, 13, 668. [Google Scholar] [CrossRef]
  8. Cao, Y.; Sun, G.; Zhai, X.; Xu, P.; Ma, L.; Deng, M.; Zhao, Z.; Yang, H.; Dong, Y.; Shang, Z.; et al. Genomic insights into the fast growth of paulownias and the formation of Paulownia witches’ broom. Mol. Plant 2021, 14, 1668–1682. [Google Scholar] [CrossRef] [PubMed]
  9. Yue, H.N.; Wu, Y.F.; Shi, Y.Z.; Wu, K.K.; Li, Y.R. First report of paulownia witches’ broom phytoplasma in China. Plant Dis. 2008, 92, 1134. [Google Scholar] [CrossRef]
  10. Tokushige, Y. Witches’ broom of Paulownia tomentosa L. J. Fac. Agric. Kyushu Univ. 1951, 10, 45–67. [Google Scholar] [CrossRef]
  11. Zhu, B. Current status of paulownia witches’ broom research. J. Shandong For. Sci. Technol. 1986, 2, 1–6. [Google Scholar]
  12. Jung, H.-Y.; Win, N.K.K.; Kim, Y.-H. Current status of phytoplasmas and their related diseases in Korea. Plant Pathol. J. 2012, 28, 239–247. [Google Scholar] [CrossRef]
  13. Doi, Y.; Teranaka, M.; Yora, K.; Asuyama, H. Mycoplasma-or PLT group-like microorganisms found in the phloem elements of plants infected with mulberry dwarf, potato witches’ broom, aster yellows, or paulownia witches’ broom. Jpn. J. Phytopathol. 1967, 33, 259–266. [Google Scholar] [CrossRef]
  14. International Committee on Systematic Bacteriology Subcommittee on the Taxonomy of Mollicutes: Minutes of the Interim Meetings, 1 and 2 August 1992, Ames, Iowa. Int. J. Syst. Bacteriol. 1993, 43, 394–397. [CrossRef]
  15. IRPCM. ‘Candidatus Phytoplasma’, a taxon for the wall-less, non-helical prokaryotes that colonize plant phloem and insects. Int. J. Syst. Evol. Microbiol. 2004, 54, 1243–1255. [Google Scholar] [CrossRef] [PubMed]
  16. Jin, K.X. Study of witches’ broom on paulownia. Acta Phytophyl. Sin. 1980, 7, 177–182. [Google Scholar]
  17. Li, Z.N.; Zhang, L.; Zhao, L.; Wu, Y.F. A new phytoplasma associated with witches’ broom on Japanese maple in China. For. Pathol. 2012, 42, 371–376. [Google Scholar] [CrossRef]
  18. Chang, W.; Li, X.; Shao, Y.; Xu, J.; Zhu, X. Molecular identification of the phytoplasma associated with kerria witches’ broom. Acta Phytopathol. Sin. 2012, 42, 541–545. [Google Scholar]
  19. Gao, J. Molecular Detection and Identification of Two Phytoplasma Diseases. Master’s Thesis, Hunan Agricultural University, Changsha, China, 2009. [Google Scholar]
  20. Li, Z.; Zhang, L.; Liu, P.; Bai, Y.; Wu, Y. First report of an aster yellows phytoplasma as the cause of rose balsam phyllody in China. J. Phytopathol. 2011, 159, 799–801. [Google Scholar] [CrossRef]
  21. Gao, R.; Zhang, G.M.; Lan, Y.F.; Zhu, T.S.; Yu, X.Q.; Zhu, X.P.; Li, X.D. Molecular characterization of phytoplasma associated with rose witches’ broom in China. J. Phytopathol. 2007, 156, 93–98. [Google Scholar] [CrossRef]
  22. Liu, J.; Chang, W.C.; Zhu, T.S.; Gao, R.; Wang, J.; Li, X.D. First report of ‘Candidatus Phytoplasma asteris’ subgroup 16SrI-D associated with Rosa xanthina witches’ broom in China. Plant Dis. 2018, 102, 1848. [Google Scholar] [CrossRef]
  23. Li, Z.N.; Min, H.; Yan, Y.; Zhao, Z.; Wu, W.J.; Wu, Y.F. First report of Syringa oblata and S. reticulata leafroll disease in China. Plant Dis. 2009, 93, 322. [Google Scholar] [CrossRef]
  24. Zhang, C.P.; Wu, K.K.; Li, Z.N.; Zhang, J.; Wang, W.L.; Wu, Y.F. Occurrence of an aster yellows (16SrI) group phytoplasma associated with a leaf roll disease of shinyleaf yellowhorn in China. Plant Pathol. 2009, 58, 790. [Google Scholar] [CrossRef]
  25. Sahashi, N.; Nakamura, H.; Yoshikawa, N.; Kubono, T.; Shoji, T.; Takahashi, T. Distribution and seasonal variation in detection of phytoplasma in bark phloem tissues of single paulownia trees infected with witches’ broom. Jpn. J. Phytopathol. 1995, 61, 481–484. [Google Scholar] [CrossRef]
  26. Cao, Y.B.; Zhai, X.Q.; Jie, D.W.; Fan, G.Q. Impact of annual temperature variation on distribution and year-round concentration variation of paulownia witches’ broom phytoplasma. J. Henan Agric. Sci. 2016, 45, 85–88. [Google Scholar]
  27. Nakamura, H.; Ohgake, S.; Sahashi, N.; Yoshikawa, N.; Kubono, T.; Takahashi, T. Seasonal variation of paulownia witches’-broom phytoplasma in paulownia trees and distribution of the disease in the Tohoku district of Japan. J. For. Res. 1998, 3, 39–42. [Google Scholar] [CrossRef]
  28. Kong, D.Z.; Lin, C.L.; Yu, S.S.; Tian, G.Z.; Ma, H.B.; Wang, S.J. Molecular diversity and evolutionary relatedness of paulownia witches’ broom phytoplasma in different geographical distributions in China. Biology 2022, 11, 1611. [Google Scholar] [CrossRef] [PubMed]
  29. Jin, K.X.; Liang, C.J.; Deng, D.L. A study of the insect vectors of witches’ broom in paulownia trees. Linye Keji Tongxun 1981. [Google Scholar]
  30. Hiruki, C. Paulownia witches’ broom important in East Asia. Acta Hortic. 1999, 496, 63–68. [Google Scholar] [CrossRef]
  31. La, Y.J.; Park, W.C. Insect transmission of paulownia witches’ broom mycoplasma-like organism to periwinkle plant by tobacco leaf bug, Cyrtopeltis tenuis Reuter. Korean J. Plant Pathol. 1994, 10, 211–214. [Google Scholar]
  32. Yeo, W.H.; Bak, W.C.; Lee, J.H.; Koh, M.G.; Yi, C.K.; Kim, Y.H. Transmission of paulownia witches’ broom mycoplasma-like organisms to periwinkle by a leafhopper, Empoasca sp. J. Korean Soc. For. Sci. 1994, 83, 1–5. [Google Scholar]
  33. Jin, K.X.; Gao, Z.H. Insect vector of jujube witches’ broom, Hishimonoides chinensis, transmit paulownia witches’ broom. For. Sci. Technol. 1984, 15, 22–24. [Google Scholar]
  34. Jin, K.X.; Fu, C.S.; Li, Z.L.; Zhang, W.J. Study on the pathogen and transmission pathway of paulownia witches’ broom. Sci. Silvae Sin. 1978, 14, 1–4. [Google Scholar]
  35. Hoshi, A.; Oshima, K.; Kakizawa, S.; Ishii, Y.; Ozeki, J.; Hashimoto, M.; Komatsu, K.; Kagiwada, S.; Yamaji, Y.; Namba, S. A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. Proc. Natl. Acad. Sci. USA 2009, 106, 6416–6421. [Google Scholar] [CrossRef] [PubMed]
  36. Jiang, J.P. Paulownia Cultivation Science; China Forestry Publishing House: Beijing, China, 1990. [Google Scholar]
  37. Yang, J.X. The uptake of phosphorus and potassium in diseased twigs and leaves of paulownia witches’ broom by using 32P and Rb86. Sci. Silvae Sin. 1989, 25, 167–170. [Google Scholar]
  38. Hu, Q.X.; Zhou, Y.Z.; Ding, D.M. Changes of the phenol content and enzyme of witches’ broom diseased paulownia. For. Pest Dis. 1991, 2, 9–11. [Google Scholar]
  39. Fan, G.Q.; Jiang, J.P. Study on the relation between witches’ broom protein and amino acid change in paulownia leaves. For. Res. 1997, 10, 570–573. [Google Scholar]
  40. Ju, G.S.; Wang, R.; Zhou, Y.L.; Ruan, D.J. Study on the relationship between the content of vitamin C and resistance of Paulownia spp. to witches’ broom. For. Res. 1996, 9, 431–434. [Google Scholar]
  41. Zhao, H.J.; Wu, G.Y.; Lin, X.W.; Huang, Z.L. Relationship between witches’ broom of paulownia and superoxide dismutase. Plant Phsiology Commun. 1995, 31, 266–267. [Google Scholar]
  42. Jiang, J.P.; Zhu, J.J.; Liu, T.Z.; WU, L.G. Preliminary study on the relationship between paulownia witches’ broom and peroxidase. Acta Agric. Univ. Henanensis 1993, 27, 301–304. [Google Scholar]
  43. Jiang, J.P.; Liu, T.Z.; Wang, Z.T. The seasonal changes of peroxidase isozyme in paulownia with witches’ broom disease. Acta Agric. Univ. Henanensis 1996, 30, 123–126. [Google Scholar]
  44. Song, X.B.; Zhang, X.W.; Zheng, W.F.; Ao, H.Y.; Ren, F.J. An anatomical observation of organ structure of paulownia infected by witches’ broom. Shaanxi For. Sci. Technol. 1993, 4, 38–40. [Google Scholar]
  45. Chen, Y.M. Detrimental effects of witches’ broom on microstructure physio-biochemical nature of leaves and wood properties of paulownia. J. Northwest For. Collge 1992, 7, 38–40. [Google Scholar]
  46. Zhai, X.Q.; Cao, X.B.; Fan, G.Q. Growth of paulownia witches’ broom seedlings treated with methylmethane sulphonate and SSR analysis. Sci. Silvae Sin. 2010, 46, 176–181. [Google Scholar]
  47. Cao, X.B.; Fan, G.Q.; Zhai, X.Q. Morphological changes of the witches’ broom seedlings of Paulownia tomentosa treated with methyl methanesulphonate and SSR analysis. Acta Phytopathol. Sin. 2012, 42, 214–218. [Google Scholar]
  48. Cao, X.B.; Fan, G.Q.; Deng, M.J.; Zhao, Z.L.; Dong, Y.P. Identification of genes related to paulownia witches’ broom by AFLP and MSAP. Int. J. Mol. Sci. 2014, 15, 14669–14683. [Google Scholar] [CrossRef] [PubMed]
  49. Cao, X.B.; Fan, G.Q.; Zhao, Z.L.; Deng, M.J.; Dong, Y.P. Morphological changes of paulownia seedlings infected phytoplasmas reveal the genes associated with witches’ broom through AFLP and MSAP. PLoS ONE 2014, 9, e112533. [Google Scholar] [CrossRef]
  50. Li, M.; Zhai, X.Q.; Fan, G.Q.; Zhang, B.L.; Liu, F. Effect of oxytetracycline on the morphology of seedling with witches’ broom and DNA methylation level of Paulownia tomentosa×P. Fortunei. Sci. Silvae Sin. 2008, 44, 152–156. [Google Scholar]
  51. Mou, H.Q.; Lu, J.; Zhu, S.F.; Lin, C.L.; Tian, G.Z.; Xu, X.; Zhao, W.J. Transcriptomic analysis of paulownia infected by paulownia witches’ broom phytoplasma. PLoS ONE 2013, 8, e77217. [Google Scholar] [CrossRef]
  52. Liu, R.; Dong, Y.; Fan, G.; Zhao, Z.; Deng, M.; Cao, X.; Niu, S. Discovery of genes related to witches’ broom disease in Paulownia tomentosa x Paulownia fortunei by a de novo assembled transcriptome. PLoS ONE 2013, 8, e80238. [Google Scholar] [CrossRef]
  53. Fan, G.; Dong, Y.; Deng, M.; Zhao, Z.; Niu, S.; Xu, E. Plant-pathogen interaction, circadian rhythm, and hormone-related gene expression provide indicators of phytoplasma infection in Paulownia fortunei. Int. J. Mol. Sci. 2014, 15, 23141. [Google Scholar] [CrossRef] [PubMed]
  54. Fan, G.; Xu, E.; Deng, M.; Zhao, Z.; Niu, S. Phenylpropanoid metabolism, hormone biosynthesis and signal transduction-related genes play crucial roles in the resistance of Paulownia fortunei to paulownia witches’ broom phytoplasma infection. Genes Genom. 2015, 37, 913–929. [Google Scholar] [CrossRef]
  55. Fan, G.; Cao, X.; Zhao, Z.; Deng, M. Transcriptome analysis of the genes related to the morphological changes of Paulownia tomentosa plantlets infected with phytoplasma. Acta Physiol. Plant. 2015, 37, 1–12. [Google Scholar] [CrossRef]
  56. Dong, Y.P.; Zhang, H.Y.; Fan, G.Q.; Zhai, X.Q.; Wang, Z.; Cao, Y.B. Comparative transcriptomics analysis of phytohormone-related genes and alternative splicing events related to witches’ broom in paulownia. Forests 2018, 9, 318. [Google Scholar] [CrossRef]
  57. Fan, G.; Cao, X.; Niu, S.; Deng, M.; Zhao, Z.; Dong, Y. Transcriptome, microRNA, and degradome analyses of the gene expression of paulownia with phytoplasma. BMC Genom. 2015, 16, 896. [Google Scholar] [CrossRef] [PubMed]
  58. Li, B.; Zhai, X.; Cao, Y.; Zhao, H.; Wang, Z.; Liu, H.; Fan, G. Transcriptome and small RNA sequencing analysis revealed roles of PaWB-related miRNAs and genes in Paulownia fortunei. Forests 2018, 8, 397. [Google Scholar] [CrossRef]
  59. Zhao, X.; Cao, X.; Cao, Y.; Zhao, Z.; Fan, G. Integrated full-length transcriptome and metabolome analysis of the early defense mechanisms in paulownia witches’ broom disease. J. Hortic. Sci. Biotechnol. 2023, 98, 342–354. [Google Scholar] [CrossRef]
  60. Fan, G.Q.; Niu, S.Y.; Xu, T.; Deng, M.J.; Zhao, Z.L.; Wang, Y.L.; Cao, L.; Wang, Z. Plant-Pathogen interaction-related microRNAs and their targets provide indicators of phytoplasma infection in Paulownia tomentosa x Paulownia fortunei. PLoS ONE 2015, 10, e0140590. [Google Scholar] [CrossRef] [PubMed]
  61. Fan, G.; Niu, S.; Zhao, Z.; Deng, M.; Xu, E.; Wang, Y.; Yang, L. Identification of microRNAs and their targets in Paulownia fortunei plants free from phytoplasma pathogen after methyl methane sulfonate treatment. Biochimie 2016, 127, 271–280. [Google Scholar] [CrossRef]
  62. Niu, S.Y.; Fan, G.Q.; Deng, M.J.; Zhao, Z.L.; Xu, E.K.; Cao, L. Discovery of microRNAs and transcript targets related to witches’ broom disease in Paulownia fortunei by high-throughput sequencing and degradome approach. Mol. Genet. Genom. 2016, 291, 181–191. [Google Scholar] [CrossRef]
  63. Cao, X.B.; Zhai, X.Q.; Zhang, Y.F.; Cheng, Z.Y.; Li, X.Y.; Fan, G.Q. Comparative analysis of microRNA expression in three paulownia species with phytoplasma infection. Forests 2018, 9, 302. [Google Scholar] [CrossRef]
  64. Wang, Z.; Zhai, X.Q.; Cao, Y.B.; Dong, Y.P.; Fan, G.Q. Long Non-Coding RNAs Responsive to witches’ broom disease in Paulownia tomentosa. Forests 2017, 8, 348. [Google Scholar] [CrossRef]
  65. Cao, Y.B.; Fan, G.Q.; Zhai, X.Q.; Dong, Y.P. Genome-wide analysis of lncRNAs in Paulownia tomentosa infected with phytoplasmas. Acta Physiol. Plant. 2018, 40, 49. [Google Scholar] [CrossRef]
  66. Fan, G.Q.; Cao, Y.B.; Wang, Z. Regulation of Long Noncoding RNAs Responsive to phytoplasma infection in Paulownia tomentosa. Int. J. Genom. 2018, 2018, 1–16. [Google Scholar] [CrossRef] [PubMed]
  67. Fan, G.Q.; Wang, Z.; Zhai, X.Q.; Cao, Y.B. ceRNA Cross-talk in paulownia witches’ broom disease. Int. J. Mol. Sci. 2018, 19, 2463. [Google Scholar] [CrossRef]
  68. Xu, P.; Huang, S.; Zhai, X.; Fan, Y.; Li, X.; Yang, H.; Cao, Y.; Fan, G. N6-methyladenosine modification changes during the recovery processes for paulownia witches’ broom disease under the methyl methanesulfonate treatment. Plant Direct 2023, 7, e508. [Google Scholar] [CrossRef] [PubMed]
  69. Cao, X.B.; Fan, G.Q.; Dong, Y.P.; Zhao, Z.L.; Deng, M.J.; Wang, Z.; Liu, W.S. Proteome profiling of paulownia seedlings infected with phytoplasma. Front. Plant Sci. 2017, 8, 342. [Google Scholar] [CrossRef]
  70. Wang, Z.; Liu, W.; Fan, G.; Zhai, X.; Zhao, Z.; Dong, Y.; Deng, M.; Cao, Y. Quantitative proteome-level analysis of paulownia witches’ broom disease with methyl methane sulfonate assistance reveals diverse metabolic changes during the infection and recovery processes. PeerJ 2017, 5, e3495. [Google Scholar] [CrossRef]
  71. Wei, Z.; Wang, Z.; Li, X.Y.; Zhao, Z.L.; Deng, M.J.; Dong, Y.P.; Cao, X.B.; Fan, G.Q. Comparative proteomic analysis of Paulownia fortunei response to phytoplasma infection with dimethyl sulfate treatment. Int. J. Genom. 2017, 2017, 1–11. [Google Scholar] [CrossRef]
  72. Cao, Y.; Fan, G.; Wang, Z.; Gu, Z. Phytoplasma-induced changes in the acetylome and succinylome of Paulownia tomentosa provide evidence for involvement of acetylated proteins in witches’ broom disease. Mol. Cell. Proteom. 2019, 18, 1210–1226. [Google Scholar] [CrossRef]
  73. Li, B.B.; Lin, D.; Zhai, X.Q.; Fan, G.Q.; Zhao, Z.L.; Cao, X.B.; Yang, H.B.; Che, T.D.; Yuan, Z.; Liu, T. Conformational changes in three-dimensional chromatin structure in Paulownia fortunei after phytoplasma infection. Phytopathology 2022, 112, 373–386. [Google Scholar] [CrossRef] [PubMed]
  74. Yan, L.; Fan, G.; Li, X. Genome-wide analysis of three histone marks and gene expression in Paulownia fortunei with phytoplasma infection. BMC Genom. 2019, 20, 234. [Google Scholar] [CrossRef] [PubMed]
  75. Yan, L.J.; Zhai, X.Q.; Zhao, Z.L.; Fan, G.Q. Whole-genome landscape of H3K4me3, H3K36me3 and H3K9ac and their association with gene expression during paulownia witches’ broom disease infection and recovery processes. 3 Biotech 2020, 10, 1–11. [Google Scholar] [CrossRef] [PubMed]
  76. Cao, X.B.; Zhai, X.Q.; Zhao, Z.L.; Deng, M.J.; Li, Y.S.; Fan, G.Q. Genome-wide DNA methylation analysis of paulownia with phytoplasma infection. Gene 2020, 755, 144905. [Google Scholar] [CrossRef] [PubMed]
  77. Zhang, D.F.; Deng, M.J.; Cao, Y.B.; Huang, S.M.; Zhao, X.Q.; Fan, G.Q. Identification of ARF gene family and its response to phytoplasma infection in Paulownia fortunei. Mol. Plant Breed. 2022. Available online: https://kns.cnki.net/kcms/detail/46.1068.S.20220415.2122.036.html (accessed on 19 April 2024).
  78. Fan, J.; Deng, M.; Li, B.; Fan, G. Genome-wide identification of the Paulownia fortunei Aux/IAA gene family and its response to witches’ broom caused by phytoplasma. Int. J. Mol. Sci. 2024, 25, 2260. [Google Scholar] [CrossRef] [PubMed]
  79. Zhu, P.; Fan, Y.; Xu, P.; Fan, G. Bioinformatic analysis of the BTB gene family in Paulownia fortunei and functional characterization in response to abiotic and biotic stresses. Plants 2023, 12, 4144. [Google Scholar] [CrossRef] [PubMed]
  80. Dong, Y.; Deng, M.J.; Mo, S.F.; Fan, G.Q. Identification of bZIP gene family of Paulownia fortunei and their response to pathogenic process of witches’ broom phytoplasmas. J. Henan Agric. Univ. 2023, 57, 216–230. [Google Scholar]
  81. Li, L.; Guo, N.; Cao, Y.; Zhai, X.; Fan, G. Genome-wide characterization of calmodulin and calmodulin-like protein gene families in Paulownia fortunei and identification of their potential involvement in paulownia witches’ broom. Genes 2023, 14, 1540. [Google Scholar] [CrossRef]
  82. Li, Y.; Cao, Y.; Fan, Y.; Fan, G. Comprehensive analysis of the GRAS gene family in Paulownia fortunei and the response of DELLA proteins to paulownia witches’ broom. Int. J. Mol. Sci. 2024, 25, 2425. [Google Scholar] [CrossRef]
  83. Deng, M.; Dong, Y.; Xu, S.; Huang, S.; Zhai, X.; Fan, G. Genome-wide identification and expression of the Paulownia fortunei MADS-box gene family in response to phytoplasma infection. Genes 2023, 14, 696. [Google Scholar] [CrossRef]
  84. Xu, S.S.; Cao, Y.; Cao, X.; Dong, Y.; Zhai, X.Q.; Fan, G.Q. Analysis of the NCED gene family in Paulownia fortunei and their response to witches’ broom phytoplasmas. J. Henan Agric. Univ. 2022, 56, 968–978. [Google Scholar]
  85. Lang, Y.Q.; Zhai, X.Q.; Cao, X.B.; Fan, G.Q. Analysis of paulownia NLR gene family and their response to phytoplasmas. J. Southwest For. Univ. 2024, 44, 7–20. [Google Scholar] [CrossRef]
  86. Zhao, Z.; Zhang, P.; Deng, M.; Cao, Y.; Fan, G. Genome-wide identification and expression analyses of the PP2C gene family in Paulownia fortunei. Forests 2023, 14, 207. [Google Scholar] [CrossRef]
  87. Zhao, T.; Fan, Y.; Cao, Y.; Zhao, X.; Fan, G. Identification of the SERK Gene family in Paulownia fortunei and its involvement in the response to biotic and abiotic stresses. Phyton-Int. J. Exp. Bot. 2023, 92, 2473–2488. [Google Scholar] [CrossRef]
  88. Yang, H.; Zhai, X.; Zhao, Z.; Fan, G. Comprehensive analyses of the SPL transcription factor family in Paulownia fortunei and their responses to biotic and abiotic stresses. Int. J. Biol. Macromol. 2023, 226, 1261–1272. [Google Scholar] [CrossRef] [PubMed]
  89. Han, J.X.; Cao, X.B.; Liu, H.F.; Fan, G.Q. Analysis genes in the Paulownia fortunei TCP family and their response to witches’ broom and drought stress. J. For. Environ. 2022, 42, 337–345. [Google Scholar]
  90. Jiang, X.Y.; Cao, X.B.; Zhao, Z.L.; Deng, M.J.; Fan, G.Q. Analysis of E2 gene family in paulownia and their response to witches’ broom phytoplasmas. J. For. Environ. 2022, 42, 174–183. [Google Scholar]
  91. Chang, M.Y.; Cao, X.B.; Zhao, Z.L.; Fan, G.Q. Identification of the WPR gene family in paulownia and its response to witches’ broom phytoplasma. J. For. Environ. 2022, 42, 312–319. [Google Scholar]
  92. Brant, E.J.; Budak, H. Plant small non-coding RNAs and their roles in biotic stresses. Front. Plant Sci. 2018, 9, 1038. [Google Scholar] [CrossRef]
  93. Wierzbicki, A.T.; Blevins, T.; Swiezewski, S. Long noncoding RNAs in plants. Ann. Rev. Plant Biol. 2021, 72, 245–271. [Google Scholar] [CrossRef]
  94. Shen, L.; Liang, Z.; Wong, C.E.; Yu, H. Messenger RNA modifications in plants. Trends Plant Sci. 2019, 24, 328–341. [Google Scholar] [CrossRef] [PubMed]
  95. Candela-Ferre, J.; Diego-Martin, B.; Perez-Alemany, J.; Gallego-Bartolome, J. Mind The gap: Epigenetic regulation of chromatin accessibility in plants. Plant Physiol. 2024, 194, 1998–2016. [Google Scholar] [CrossRef] [PubMed]
  96. Berlec, A. Novel techniques and findings in the study of plant microbiota: Search for plant probiotics. Plant Sci. 2012, 193–194, 96–102. [Google Scholar] [CrossRef] [PubMed]
  97. Huang, J.; Li, X.Z.; Fan, G.Q. Analysis fungal endophytes community structure in paulownia witches’ broom disease based on random forest machine learning method. J. Henan Agric. Univ. 2023, 57, 776–783. [Google Scholar]
  98. Li, X.; Huang, J.; Zhai, X.; Zhao, Z.; Pan, Y.; Fan, G. Bacterial assembly as part of immnue system in paulownia responses to witches’ broom caused by phytoplasmas. Res. Sq. 2022. [Google Scholar] [CrossRef]
  99. Li, R.X.; Cheng, S.R.; Liu, T.Z.; Zhang, Z.Y. The resistant difference of paulownia on witches’ broom and natural appraisal. J. Henan Agric. Univ. 1987, 21, 170–176. [Google Scholar]
  100. Yang, J.X.; Zhang, G.L.; Fan, J.F.; Zhou, Y.X.; Wang, P.X.; Li, Y.Z.; Li, W.A. Investigation on phytoplasma disease in different species and provenance of the genus Paulownia. J. Northwest For. Univ. 2005, 20, 115–116. [Google Scholar]
  101. Ren, G.L.; Liu, T.Z.; Zheng, L.C.; Shi, X.Y.; Zheng, T.M.; Kong, L.L.; Zhang, S.S.; Wang, K.J.; Dong, X.L.; Jiao, S.L.; et al. Study on induced resistance of paulownia to witches’ broom: I resistance induced by inoculating the pathogenic MLO. J. Henan Agric. Univ. 1994, 28, 240–244. [Google Scholar]
  102. Ren, G.L.; Liu, T.Z.; Shi, X.Y.; Tian, G.H.; Zhang, S.S.; Wei, L.D.; Dong, X.L. Study on induced resistance of paulownia to witches’ broom. J. Henan Agric. Univ. 1995, 29, 378–381. [Google Scholar]
  103. Zhang, G.L.; Wang, P.X.; Li, Y.Z.; Li, W.A.; Yang, H.P.; Yang, J.X. Disease resistance selection through radiomutagenesis to the Paulownia. J. Northwestern For. Univ. 2006, 21, 130–132. [Google Scholar]
  104. Bertaccini, A. Containment of phytoplasma-associated plant diseases by antibiotics and other antimicrobial molecules. Antibiotics 2021, 10, 1398. [Google Scholar] [CrossRef] [PubMed]
  105. La, Y.J.; Shin, H.D. Field control of paulownia witches’ broom with oxytetracycline hydrochloride. J. Korean Soc. For. Sci. 1980, 49, 6–10. [Google Scholar]
  106. Miao, J.B.; SiMa, C.; Ge, S.X.; Huai, J.S.; Zhang, S.M. Preliminary report on treatment of paulownia witches’ broom disease by soaking root in warm water. J. Henan Agric. Sci. 1982, 01, 32. [Google Scholar]
  107. Tong, D.Q.; Li, Z.L. Several problems in the prevention and control of paulownia witches’ broom disease. J. Shandong For. Sci. Technol. 1990, 2, 42–44. [Google Scholar]
  108. Wang, X.-Y.; Zhang, R.Y.; Li, J.; Li, Y.-H.; Shan, H.-L.; Li, W.-F.; Huang, Y.-K. The diversity, distribution and status of phytoplasma diseases in China. Front. Sustain. Food Syst. 2022, 6, 943080. [Google Scholar] [CrossRef]
  109. Sugio, A.; Kingdom, N.-H.; MacLean, A.-M.; Grieve, V.-M.; Hogenhout, S.-A. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc. Natl. Acad. Sci. USA 2011, 108, E1254–E1263. [Google Scholar] [CrossRef]
  110. Huang, W.-J.; MacLean, A.-M.; Sugio, A.; Maqbool, A.; Busscher, M.; Cho, S.-T.; Kamoun, S.; Kuo, S.-H.; Immink, R.-G.; Hogenhout, S.A. Parasitic modulation of host development by ubiquitin-independent protein degradation. Cell 2021, 184, 5201–5214.e12. [Google Scholar] [CrossRef]
Microorganisms 12 00885 g001
Figure 1. Typical symptoms of PaWB phytoplasma-infected Paulownia spp. (a) Healthy tree, (b) diseased tree, (c) healthy branches, (d) diseased branches, (e) comparison of healthy tree (left) and diseased tree (right).
Figure 1. Typical symptoms of PaWB phytoplasma-infected Paulownia spp. (a) Healthy tree, (b) diseased tree, (c) healthy branches, (d) diseased branches, (e) comparison of healthy tree (left) and diseased tree (right).
Microorganisms 12 00885 g001
Microorganisms 12 00885 g002
Figure 2. Frame diagram of the PaWB phytoplasma molecular pathogenic mechanism. The phytoplasma multiplies in the sieve cells of the phloem, from which it secret effector proteins to neighbor tissue cells. The frame contains three levels, namely DNA/genome level, RNA/transcriptome level and the protein/proteome level. The mapped gene expression regulation, through genetic information flow according to DNA, RNA and protein, is shown together with the epigenetic modifications and the interaction of the phytoplasma effector SAP54PaWB and the target protein PfSPLa (Paulownia fortunei SQUAMOSA-PRO-MOTER BINDING PROTEIN-LIKE a). Dotted lines show potential regulation clues.
Figure 2. Frame diagram of the PaWB phytoplasma molecular pathogenic mechanism. The phytoplasma multiplies in the sieve cells of the phloem, from which it secret effector proteins to neighbor tissue cells. The frame contains three levels, namely DNA/genome level, RNA/transcriptome level and the protein/proteome level. The mapped gene expression regulation, through genetic information flow according to DNA, RNA and protein, is shown together with the epigenetic modifications and the interaction of the phytoplasma effector SAP54PaWB and the target protein PfSPLa (Paulownia fortunei SQUAMOSA-PRO-MOTER BINDING PROTEIN-LIKE a). Dotted lines show potential regulation clues.
Microorganisms 12 00885 g002
Table 2. Identification of paulownia gene families and PaWB-related paulownia genes.
Table 2. Identification of paulownia gene families and PaWB-related paulownia genes.
Gene FamilyData SetsFamily MembersPaWB-Related GenesReferences
ARF, auxin response factorPRJNA62426433PfARF 18, 21[77]
Aux/IAA, auxin/indole-3-acetic acid 62PfAux/IAA 13, 33, 45[78]
BTB, Bric-a-Bric/Tramtrack/Broad complexPRJNA62426462PfBTB 3, 12, 14, 16, 19, 36, 44[79]
bZIP, basic leucine zipperPRJNA62426489PfbZIP 46[80]
CaM/CML, calmodulin and calmodulin-like proteinPRJNA62426463
(5 CaMs, 58 CMLs)		 [81]
GRAS, GAI//RGA//SCL 79PfGRAS 12[82]
MADS-boxPRJNA79402789PfMADS3, 57, 87[83]
NCED, 9-cis-epoxycarotenoid dioxygenasePRJNA62426428PfNCED16[84]
NLR, nucleotide-binding leucine-rich repeat receptors PRJNA624264199PfNLR 181[85]
PP2C, protein phosphatase 2C 91PfPP2C 2, 12, 19, 80[86]
SERK, somatic embryogenesis receptor-like kinasesPRJNA62426412PfSERK3, 11[87]
SPL, SQUAMOSA-PRO-MOTER BINDING PROTEIN-LIKEPRJNA433928, PRJNA221355,
PRJNA289582, SRP060682		23PfSPL 1, 4, 5, 9, 10, 11, 12, 13, 17, 18[88]
TCP, teosinte branched1, cycloidea, proliferating cell factors 35PfTCP 17, 27[89]
UBC E2, ubiquitin-conjugating enzyme E2PRJNA62426456PfUBC 44, 45, 51[90]
WPR, WEB1/PMI2-related 16PfWEB 3, PfWPRb 2, PfWPRb 3, PfPMI 2[91]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhang, Y.; Qiao, Z.; Li, J.; Bertaccini, A. Paulownia Witches’ Broom Disease: A Comprehensive Review. Microorganisms 2024, 12, 885. https://doi.org/10.3390/microorganisms12050885

AMA Style

Zhang Y, Qiao Z, Li J, Bertaccini A. Paulownia Witches’ Broom Disease: A Comprehensive Review. Microorganisms. 2024; 12(5):885. https://doi.org/10.3390/microorganisms12050885

Chicago/Turabian Style

Zhang, Yajie, Zesen Qiao, Jidong Li, and Assunta Bertaccini. 2024. "Paulownia Witches’ Broom Disease: A Comprehensive Review" Microorganisms 12, no. 5: 885. https://doi.org/10.3390/microorganisms12050885

APA Style

Zhang, Y., Qiao, Z., Li, J., & Bertaccini, A. (2024). Paulownia Witches’ Broom Disease: A Comprehensive Review. Microorganisms, 12(5), 885. https://doi.org/10.3390/microorganisms12050885

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop