The parasitic bacterium phytoplasma is a master manipulator. It turns its hosts into sterile ‘zombie’ plants that remain alive only to support the parasite. Phytoplasma secretes a protein called SAP54, which transforms the flowers of the plants into leaf-like structures. Until recently, scientists believed this transformation was how the parasite attracted tiny sap-feeding insects called leafhoppers, which act as vectors that transport phytoplasma to its next host. However, more recent research has shown that the transformation of flowers into leaf-like structures is not needed to lure leafhoppers to the plant. So, what is it about SAP54 that manipulates the preferences of leafhoppers?

To find out, Orlovskis et al. genetically modified plants to produce SAP54. They then carefully observed the number of male and female leafhoppers attracted to the mutant plants compared to plants that had not been genetically manipulated. They also used genetic analysis to investigate the proteins controlling the plant’s defence mechanisms.

Orlovskis et al. found that SAP54 attracted female leafhoppers to the leaves of the plant, but only when males were also present. SAP54 also suppressed the plant’s defences when males were on the leaves, making the plant more inviting to females. Increasing the number of females naturally facilitates breeding, resulting in more insects that can transport the parasite to new host plants.

A plant protein, called SHORT VEGETATIVE PHASE (or SVP for short), turned out to be critical in this process. Orlovskis et al. discovered that SAP54 promotes the breakdown of SVP, and plants lacking this protein also attracted more females when exposed to male leafhoppers. This suggests that SAP54 acts as a ‘molecular matchmaker’, helping male leafhoppers find mates by breaking down SVP in leaves. The involvement of SVP in attracting leafhoppers is surprising, as the family of proteins which SVP belongs to is primarily known for regulating developmental processes, such as flowering, rather than influencing how plants interact with their environment.

These findings deepen our understanding of the complex relationships between parasites, plants and insects, demonstrating how parasites manipulate both plant biology and insect behaviour. This knowledge could inform new strategies for controlling plant diseases spread by insects, potentially reducing crop losses caused by phytoplasma.

Parasites often excel in altering the development and behavior of their hosts, a trait essential for their survival and propagation. The trait is particularly pronounced in obligate parasites, which have substantial control over their hosts, earning them the nickname 'puppet masters'. The phenomenon exemplifies the concept of extended phenotypes (originally coined by Dawkins, 1982), where the impact of an organism’s genes extends beyond its own physical form and affects other organisms. This concept is especially evident in obligate parasites that depend on alternate hosts for transmission, as they often do not only alter the conditions of their immediate hosts but also have far-reaching effects on other organisms in the ecosystem.

For instance, the protozoan parasite Taxoplasma gondii changes the behavior of their intermediate rodent hosts by reducing their innate fear for cats, which are the definite hosts where the parasite undergoes sexual reproduction to produce oocysts (Tong et al., 2021). Similarly, the rust fungus Puccinia monoica induces its host plant, Boechera stricta, to produce 'pseudoflowers'. These structures mimic real flowers and attract pollinators with their scent and sugary rewards, an essential strategy for the fungus to spread its spores between plants (Roy, 1993; Cano et al., 2013). Although advancements have been made in identifying parasite virulence factors, our understanding of the specific host processes that are commandeered to produce these extended phenotypes is still developing.

Parallel to these discoveries are the studies on the extended phenotypes of phytoplasmas, which have revealed that their manipulative abilities stem from particular genes within these pathogens (Sugio et al., 2011b; Tomkins et al., 2018; Huang et al., 2020; Wang et al., 2024). Phytoplasmas cause disease in crops, ornamentals and native plants worldwide (Kumari et al., 2019) and are often dependent on sap-feeding insects, including leafhoppers, plant hoppers and psyllids, for transmission (Weintraub and Beanland, 2006). As obligate bacterial parasites, phytoplasmas frequently trigger the emergence of unusual plant structures such as leaf-like floral parts (phyllody) and the excessive growth and clustering of leaves and branches (witch’s broom; Lee et al., 2000; Al-Subhi et al., 2018; Kumari et al., 2019). These alterations not only compromise plant health but also promote attraction and colonization of insect vectors that are primarily responsible for phytoplasma spread and transmission (Sugio et al., 2011a; Frost et al., 2013; MacLean et al., 2014; Orlovskis and Hogenhout, 2016; Clements et al., 2021; Al-Subhi et al., 2021; Huang and Hogenhout, 2022). The responsible phytoplasma genes encode for effector molecules that, once inside the plant cell cytoplasm, target and typically disrupt or degrade essential plant transcription factors involved in growth, development, and defence (review by Wang et al., 2024 and references therein as well as Liu et al., 2023; Suzuki et al., 2024; Correa Marrero et al., 2024; Yan et al., 2024; Zhang et al., 2024). This molecular interference exemplifies the extended phenotype reach, affecting not just the host appearance but also its physiological and biological processes.

The interaction between the Aster Yellows strain Witches Broom (AY-WB) phytoplasma and its vector, the aster leafhopper Macrosteles quadrilineatus, offers insights into the complex interplay between parasites and hosts. The effector protein secreted AY-WB protein (SAP) 11 binds to and destabilizes class II TCP transcription factors - this action leads to changes in leaf shapes and stem proliferation, reminiscent of witches’ brooms, and altered root architecture resembling the hairy roots found in infected plants (Bai et al., 2009; Sugio et al., 2011a; Sugio et al., 2014; Lu et al., 2014; Chang et al., 2018; Pecher et al., 2019). Additionally, this effector reduces plant jasmonic acid and salicylic-acid-mediated defence responses, alters volatile organic compounds, and promotes the reproduction rates of the insect vectors (Sugio et al., 2011a; Lu et al., 2014; Tan et al., 2016). Another effector, SAP05, recruits the 26 S proteasome component RPN10, instigating the breakdown of SPL and GATA transcription factors (Huang et al., 2021; Liu et al., 2023; Yan et al., 2024; Zhang et al., 2024). This process is linked to the typical leaf and stem proliferations of witches’ brooms in phytoplasma-infected plants. The SAP05-mediated degradation of SPLs, but not GATAs, increases the attractiveness of these plants to insect vectors (Huang et al., 2021).

However, the relationship between phytoplasma SAP54/PHYL1 effectors inducing leaf-like flowers and attracting insects seems more intricate. These effectors target and disrupt MADS-box transcription factors, akin to animal HOX genes, leading to a transformation of flowers into leaf-like structures, alterations that mirror the phyllody and virescence symptoms of phytoplasma infection (MacLean et al., 2011; MacLean et al., 2014; Wang et al., 2024; Suzuki et al., 2024; Correa Marrero et al., 2024). SAP54 recruits plant 26 S proteasome shuttle factors called radiation sensitive 23 (RAD23) to break down these transcription factors (MacLean et al., 2014; Kitazawa et al., 2022; Suzuki et al., 2024). Leafhoppers prefer plants that stably produce SAP54 for reproduction and this preference phenotype requires the presence of RAD23, which is essential for both breaking down MADS-box transcription factors and inducing leaf-like flowers (MacLean et al., 2014). However, the increased reproduction of insect vectors does not depend on the presence of leaf-like flowers. Our past research showed that insects prefer SAP54 plants during the vegetative developmental phase, before flowers emerge, and even flowering SAP54 plants upon removal of the leaf-like flowers (Orlovskis and Hogenhout, 2016). Therefore, it remains unclear whether plant MADS-box transcription factors play a role in the leafhopper attraction phenotype.

MADS-box transcription factors have been predominantly studied in relation to regulation of floral transition and flower organ development. Nonetheless, factors like suppressor of overexpression of CO 1 (SOC1) and short vegetative phase (SVP) are also expressed in leaves and other organs during the A. thaliana vegetative developmental phase, and regulate processes other than orchestrating the flowering process, such as plant defence responses, as has been shown for SOC1 (Li et al., 2020). Based on these insights, we hypothesize that leafhopper attraction is influenced by MADS-box transcription factors involved in processes other than flowering.

Here, we analysed the factors influencing leafhopper colonization preference in SAP54 plants. Surprisingly, we found that colonization preference on SAP54 plants only occurs in the presence of males on leaves during choice tests. Both SAP54 and males are essential for female preference, as females did not exhibit a preference for male-exposed versus non-exposed control plants, nor for SAP54 plants versus control plants in the absence of males. In contrast, female-only presence on SAP54 plants deters colonization by other females. We noted a clear downregulation of biotic stress response pathways in male-exposed SAP54 leaves, contrasting with the upregulation observed in female-exposed SAP54 leaves and control plants exposed to both males and females. Furthermore, we found that the MADS-box transcription factor SVP is essential for female preference in male-exposed SAP54 plants. Females also prefer colonizing male-exposed svp null mutant plants over non-exposed ones. Our research sheds light on how the conserved MADS-box transcription factor SVP influences leaf susceptibility to male herbivorous insects, promoting female attraction and colonization.

Here, we investigated colonization preferences of the leafhopper vector M. quadrilineatus, the predominant vector of AY-WB phytoplasma, for plants that produce the AY-WB effector SAP54. We made the surprising discovery that female preference for SAP54 plants only occurs in the presence of males. Both SAP54 and males are necessary for this preference, as females did not show a preference in their absence. As well, SAP54 plants exposed to males display significant downregulation of biotic stress responses. We identified the MADS-box transcription factor SVP to be essential for this female preference to male-exposed SAP54 plants. Leafhopper females exhibited a preference for reproducing on svp null mutant plants, a behavior that is also contingent upon the presence of leafhopper males, and aligning with our observation that SAP54 mediates the degradation of SVP in leaves. Therefore, by characterizing a parasite effector, we revealed the crucial role of SVP in leaf susceptibility to male herbivorous insects, enhancing female attraction and colonization.

This work built on our previous findings that the leaf-like flowers are not required for the insect colonization preference and the insect vectors are predominantly attracted to the leaves and not flowers of plants (Orlovskis and Hogenhout, 2016). Here, we independently confirm these data via experiments that show a preference of the insects for A. thaliana rosettes before the onset of flowering. Therefore, a morphological change in the host may not always be responsble for the extended phenotype effect on the alternative host, which is in this case the insect vector. It is possible that the attraction of insect vectors to leaves is the primary function of SAP54, and the induction of the leaf-like flowers an evolutionary side-effect of SAP54 adaptation to target MTFs that leads to degradation of SVP. However, the prevention of seed production through the formation of leaf-like flowers likely is likely to present an advantage to phytoplasma. AY-WB phytoplasma commonly infects annual plants, where leaves naturally senesce and die off after flowering and seed production. It is probable that prolonging the longevity of their plant hosts is advantageous for phytoplasmas, particularly considering that they are not known to be seed-transmitted. Instead, phytoplasmas rely on leafhoppers, which feed on vegetative tissues, for transmission.

We found that SAP54 mediates the destabilization of SVP. However, we did not find evidence of a direct interaction between SAP54 and SVP in our Y2H analyses. An explanation of this apparent discrepancy is that MTF proteins exhibit a propensity to form diverse complexes, including homo- and hetero-dimers, as well as higher order ternary and quaternary complexes (Davies et al., 1996; Egea-Cortines et al., 1999; Hartmann et al., 2000; Honma and Goto, 2001; Immink et al., 2002; de Folter et al., 2005). Notably, SVP is known to interact with other MTFs such as SOC1, FUL, and AGL24 (de Folter et al., 2005; Gregis et al., 2009; Balanzà et al., 2014), and we previously established that SAP54 interacts with and facilitates the degradation of multiple MTFs, including SOC1, FUL, and AGL24 (MacLean et al., 2014), as is also shown for FUL and AGL24 herein (Figure 5). Moreover, our research showed that these three MTFs are expressed in leaves, with SOC1 and AGL24 showing elevated expression in SAP54 plants exposed to males (Supplementary file 9). Hence, the destabilization of SVP by SAP54 may occur through its involvement with various SVP-containing protein complexes. This intricate interaction network also provides a possible explanation for the absence of a leafhopper preference phenotype in soc1, agl24, and ful mutant plants. It suggests that the interaction of SAP54 with multiple SVP-containing ternary and quaternary MTFs, leading to their degradation, might be essential to trigger the observed phenotype.

SVP is recognized as a conserved regulator of flowering time across a variety of eudicot species, as evidenced by several studies (Sun et al., 2016; Li et al., 2016). It is expressed in the leaves during the vegetative growth stages of plants (Zheng et al., 2009; Li et al., 2016; Wu et al., 2017), which correlates with the wide host range of AY-WB phytoplasmas. While the primary role of SVP and its homologs has been associated with flowering, their involvement in additional biological processes beyond this remains underexplored (Liu et al., 2018). However, emerging research has begun to shed light on the roles of SVP outside of flowering: for instance, it acts as a positive regulator of age-related resistance against bacterial pathogens in Arabidopsis thaliana (Wilson et al., 2017) and serves as a negative regulator of various Jasmonate Zim-domain (JAZ) genes during the vegetative growth phase (Gregis et al., 2013). Our findings contribute to this expanding body of knowledge, suggesting that plant immunity may be intricately controlled by developmental regulators like SVP, which possesses multiple, diverse functions throughout plant development (Berry and Argueso, 2022 references therein). The observation that female leafhoppers prefer to reproduce on both SAP54 and svp mutant plants exclusively in the presence of leafhopper males underscores a sophisticated regulatory effect of SVP and other MADS-box transcription factors targeted by SAP54 on plant responses to the different sexes of the herbivores. This intricate interaction is detailed in the mechanism proposed in Figure 7.

Figure 7

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Considering that certain phytoplasmas can modify plant volatile production (Mayer et al., 2008a; Mayer et al., 2008b; Rid et al., 2016; Tan et al., 2016), we examined whether male-induced volatile cues play a role in attracting females. Our results suggest that female leafhopper preference for laying eggs on male-exposed SAP54 plants is unlikely to depend solely on volatiles originating from the males or induced by them (Figure 1—figure supplement 3). Thus, it is plausible that females are guided to male-occupied SAP54 and svp mutant plants through a different mechanism, possibly involving changes in leaf responses that are specifically induced to male insects. Male-exposed leaves of SAP54 and svp mutant plants shared transcriptional changes of genes involved cell wall structure processes and changes in secondary (isoprenoid) metabolism. As such, these could influence female leafhoppers’ host plant selection and their egg-laying preferences on plants exposed to males. However, given that the removal of males from SAP54 leaves prior to female choice does not enhance female colonization (comparison of Figure 1 treatment 4 with treatment 5), we cannot exclude that male produced volatiles or mating calls can enhance or supplement SAP54-dependent changes in biotic stress responses to males for enhanced female attraction.

Males and females of M. quadrilineatus, the primary vector of AY-WB phytoplasma, exhibit distinct movement and feeding behaviors, as documented by Beanland et al., 1999. Moreover, the leafhoppers, especially females, live longer on aster yellows infected plants compared to non-infected plants (Beanland et al., 2000). Here, we show that the combination of the aster yellows phytoplasma effector SAP54 and males attract females in a manner that depends on SVP. Moreover, plant biotic stress and defence responses are largely suppressed in male (compared to female) exposed SAP54 plants, and SVP also displays distinct plant transcriptional responses to male and female leafhoppers. Nevertheless, the mechanisms how male and female leafhoppers, in combination with SAP54, differentially affect plant defence responses will need further investigation. While the differences in male and female behavior may play a role (Beanland et al., 1999), there is also the possibility that effectors in the saliva of sap-feeding insects modulate plant processes, including defence (Snoeck et al., 2022), and sex-specific differences exist in the proteome of sap-feeding insect saliva (Miao et al., 2018), potentially influencing plant response. Moreover, plant immune responses initiated by the molecular patterns associated with insect eggs (EAMPs) that bear similarities to pattern-triggered immunity (PTI) activated by bacterial pathogens (Gouhier-Darimont et al., 2013) may play a role in the observed gender-specific differences.

Pathogens uniquely exploit sexual dimorphism in their hosts to enhance their dispersal and survival in nature. For example, the bacterial parasite infecting the crustacean Daphnia magna selectively uses male hosts for horizontal transmission, while exploiting females for internal replication and spore production, thus facilitating widespread disease transmission (Nørgaard et al., 2019). Toll signaling pathway contributes to the varied resistance observed between male and female Drosophila to both Gram-positive and Gram-negative bacteria (Duneau et al., 2017). Similarly, the endosymbiotic bacterium Wolbachia often exhibits distinct effects on the embryonic development of male and female gametes, showcasing another instance of pathogens leveraging host sexual differences (Serbus et al., 2008). Recent discovery identified a novel Wolbachia factor Oscar which interacts with host protein Masculinizer to inhibit masculinization and lead to male-killing in two insect species (Katsuma et al., 2022). Our study further expands the mechanistic understanding about insect gender specific factors targeted by parasites.

In our research, we have uncovered a mechanism whereby the phytoplasma effector SAP54 targets a conserved host regulator, SVP, to attract female leafhopper vectors to produce more progeny on plants exposed to leafhopper males. Given that phytoplasmas rely on leafhoppers for acquisition during feeding and subsequent transmission to other plants, SAP54 likely promotes the abundance of phytoplasma-carrying insect vectors and facilitates phytoplasma transmission. This illustrates how a bacterial gene extends its influence beyond its primary plant host to modulate the host choice and reproductive behavior of the insect vector. Such findings underscore the complexity of tripartite plant-insect-microbe interactions, wherein parasitic genes exhibit what could be termed 'hyper-extended phenotypes,' manipulating the biology of one host to facilitate transmission through another host. This research advances our understanding of plant-microbe interactions and resonates with the concept of the Extended Evolutionary Synthesis (EES), as articulated by Hunter, 2018. Within the EES framework, parasitic genes like SAP54 evolve adaptively through both natural selection and direct biochemical interactions with plant regulators, as well as through the extended functions these regulators serve in interactions with insect vectors. In this study, we found that the extended role includes enhancing the likelihood of male vectors to attract females for reproduction.

RNA-seq raw data (fastq) are uploaded to NCBI under BioProject: PRJNA1090849.

1. 1. Orlovskis Z
   2. Singh A
   3. Kliot A
   4. Huang W
   5. Hogenhout SA

   (2024) NCBI BioProject

   ID PRJNA1090849. Arabidopsis thaliana (thale cress).

   https://www.ncbi.nlm.nih.gov/bioproject?term=PRJNA1090849

1. 1. Al-Subhi AM
   2. Hogenhout SA
   3. Al-Yahyai RA
   4. Al-Sadi AM

   (2018) Detection, identification, and molecular characterization of the 16SrII-D phytoplasmas infecting vegetable and field crops in Oman

   Plant Disease 102:576–588.

   https://doi.org/10.1094/PDIS-07-17-0935-RE

   • PubMed
   • Google Scholar
2. 1. Al-Subhi AM
   2. Al-Sadi AM
   3. Al-Yahyai RA
   4. Chen Y
   5. Mathers T
   6. Orlovskis Z
   7. Moro G
   8. Mugford S
   9. Al-Hashmi KS
   10. Hogenhout SA

   (2021) Witches’ broom disease of lime contributes to phytoplasma epidemics and attracts insect vectors

   Plant Disease 105:2637–2648.

   https://doi.org/10.1094/PDIS-10-20-2112-RE

   • PubMed
   • Google Scholar
3. 1. Ammar E-D
   2. Alessandro R
   3. Shatters RG Jr
   4. Hall DG

   (2013) Behavioral, ultrastructural and chemical studies on the honeydew and waxy secretions by nymphs and adults of the Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae)

   PLOS ONE 8:e64938.

   https://doi.org/10.1371/journal.pone.0064938

   • PubMed
   • Google Scholar
4. 1. Asai T
   2. Tena G
   3. Plotnikova J
   4. Willmann MR
   5. Chiu WL
   6. Gomez-Gomez L
   7. Boller T
   8. Ausubel FM
   9. Sheen J

   (2002) MAP kinase signalling cascade in Arabidopsis innate immunity

   Nature 415:977–983.

   https://doi.org/10.1038/415977a

   • PubMed
   • Google Scholar
5. 1. Bai X
   2. Correa VR
   3. Toruño TY
   4. Ammar ED
   5. Kamoun S
   6. Hogenhout SA

   (2009) AY-WB phytoplasma secretes a protein that targets plant cell nuclei

   Molecular Plant-Microbe Interactions 22:18–30.

   https://doi.org/10.1094/MPMI-22-1-0018

   • PubMed
   • Google Scholar
6. 1. Balanzà V
   2. Martínez-Fernández I
   3. Ferrándiz C

   (2014) Sequential action of FRUITFULL as a modulator of the activity of the floral regulators SVP and SOC1

   Journal of Experimental Botany 65:1193–1203.

   https://doi.org/10.1093/jxb/ert482

   • PubMed
   • Google Scholar
7. 1. Beanland L
   2. Hoy CW
   3. Miller SA
   4. Nault LR

   (1999) Leafhopper (Homoptera: Cicadellidae) transmission of aster yellows phytoplasma: does gender matter?: Fig. 1

   Environmental Entomology 28:1101–1106.

   https://doi.org/10.1093/ee/28.6.1101

   • Google Scholar
8. 1. Beanland L
   2. Hoy CW
   3. Miller SA
   4. Nault LR

   (2000) Influence of aster yellows phytoplasma on the fitness of aster leafhopper (Homoptera: Cicadellidae)

   Annals of the Entomological Society of America 93:271–276.

   https://doi.org/10.1603/0013-8746(2000)093[0271:IOAYPO]2.0.CO;2

   • Google Scholar
9. 1. Berry HM
   2. Argueso CT

   (2022) More than growth: Phytohormone-regulated transcription factors controlling plant immunity, plant development and plant architecture

   Current Opinion in Plant Biology 70:102309.

   https://doi.org/10.1016/j.pbi.2022.102309

   • PubMed
   • Google Scholar
10. 1. Bray NL
    2. Pimentel H
    3. Melsted P
    4. Pachter L

    (2016) Near-optimal probabilistic RNA-seq quantification

    Nature Biotechnology 34:525–527.

    https://doi.org/10.1038/nbt.3519

    • PubMed
    • Google Scholar
11. 1. Cameron R
    2. Lang EB
    3. Alvarez JM

    (2014) Use of honeydew production to determine reduction in feeding by Bemisia tabaci (Hemiptera: Aleyrodidae) adults when exposed to cyantraniliprole and imidacloprid treatments

    Journal of Economic Entomology 107:546–550.

    https://doi.org/10.1603/ec13369

    • PubMed
    • Google Scholar
12. 1. Cano LM
    2. Raffaele S
    3. Haugen RH
    4. Saunders DGO
    5. Leonelli L
    6. MacLean D
    7. Hogenhout SA
    8. Kamoun S

    (2013) Major transcriptome reprogramming underlies floral mimicry induced by the rust fungus Puccinia monoica in Boechera stricta

    PLOS ONE 8:e75293.

    https://doi.org/10.1371/journal.pone.0075293

    • PubMed
    • Google Scholar
13. 1. Chang SH
    2. Tan CM
    3. Wu CT
    4. Lin TH
    5. Jiang SY
    6. Liu RC
    7. Tsai MC
    8. Su LW
    9. Yang JY

    (2018) Alterations of plant architecture and phase transition by the phytoplasma virulence factor SAP11

    Journal of Experimental Botany 69:5389–5401.

    https://doi.org/10.1093/jxb/ery318

    • PubMed
    • Google Scholar
14. 1. Clements J
    2. Bradford BZ
    3. Garcia M
    4. Piper S
    5. Huang W
    6. Zwolinska A
    7. Lamour K
    8. Hogenhout S
    9. Groves RL

    (2021) “Candidatus Phytoplasma asteris” subgroups display distinct disease progression dynamics during the carrot growing season

    PLOS ONE 16:e0239956.

    https://doi.org/10.1371/journal.pone.0239956

    • PubMed
    • Google Scholar
15. 1. Correa Marrero M
    2. Capdevielle S
    3. Huang W
    4. Al-Subhi AM
    5. Busscher M
    6. Busscher-Lange J
    7. van der Wal F
    8. de Ridder D
    9. van Dijk ADJ
    10. Hogenhout SA
    11. Immink RGH

    (2024) Protein interaction mapping reveals widespread targeting of development-related host transcription factors by phytoplasma effectors

    The Plant Journal 117:1281–1297.

    https://doi.org/10.1111/tpj.16546

    • PubMed
    • Google Scholar
16. 1. Davies B
    2. Egea-Cortines M
    3. de Andrade Silva E
    4. Saedler H
    5. Sommer H

    (1996)

    Multiple interactions amongst floral homeotic MADS box proteins

    The EMBO Journal 15:4330–4343.

    • PubMed
    • Google Scholar
17. Book

    1. Dawkins R

    (1982)

    The Extended Phenotype

    Oxford university press.

    • Google Scholar
18. 1. de Folter S
    2. Immink RGH
    3. Kieffer M
    4. Parenicová L
    5. Henz SR
    6. Weigel D
    7. Busscher M
    8. Kooiker M
    9. Colombo L
    10. Kater MM
    11. Davies B
    12. Angenent GC

    (2005) Comprehensive interaction map of the Arabidopsis MADS Box transcription factors

    The Plant Cell 17:1424–1433.

    https://doi.org/10.1105/tpc.105.031831

    • PubMed
    • Google Scholar
19. 1. Duneau DF
    2. Kondolf HC
    3. Im JH
    4. Ortiz GA
    5. Chow C
    6. Fox MA
    7. Eugénio AT
    8. Revah J
    9. Buchon N
    10. Lazzaro BP

    (2017) The Toll pathway underlies host sexual dimorphism in resistance to both Gram-negative and Gram-positive bacteria in mated Drosophila

    BMC Biology 15:124.

    https://doi.org/10.1186/s12915-017-0466-3

    • PubMed
    • Google Scholar
20. 1. Egea-Cortines M
    2. Saedler H
    3. Sommer H

    (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus

    The EMBO Journal 18:5370–5379.

    https://doi.org/10.1093/emboj/18.19.5370

    • PubMed
    • Google Scholar
21. 1. Frost KE
    2. Esker PD
    3. Van Haren R
    4. Kotolski L
    5. Groves RL

    (2013) Factors influencing aster leafhopper (Hemiptera: Cicadellidae) abundance and aster yellows phytoplasma infectivity in Wisconsin carrot fields

    Environmental Entomology 42:477–490.

    https://doi.org/10.1603/EN12239

    • PubMed
    • Google Scholar
22. 1. Gouhier-Darimont C
    2. Schmiesing A
    3. Bonnet C
    4. Lassueur S
    5. Reymond P

    (2013) Signalling of Arabidopsis thaliana response to Pieris brassicae eggs shares similarities with PAMP-triggered immunity

    Journal of Experimental Botany 64:665–674.

    https://doi.org/10.1093/jxb/ers362

    • PubMed
    • Google Scholar
23. 1. Gregis V
    2. Sessa A
    3. Colombo L
    4. Kater MM

    (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis

    The Plant Cell 18:1373–1382.

    https://doi.org/10.1105/tpc.106.041798

    • PubMed
    • Google Scholar
24. 1. Gregis V
    2. Sessa A
    3. Dorca-Fornell C
    4. Kater MM

    (2009) The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes

    The Plant Journal 60:626–637.

    https://doi.org/10.1111/j.1365-313X.2009.03985.x

    • PubMed
    • Google Scholar
25. 1. Gregis V
    2. Andrés F
    3. Sessa A
    4. Guerra RF
    5. Simonini S
    6. Mateos JL
    7. Torti S
    8. Zambelli F
    9. Prazzoli GM
    10. Bjerkan KN
    11. Grini PE
    12. Pavesi G
    13. Colombo L
    14. Coupland G
    15. Kater MM

    (2013) Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during VEGETATIVE and reproductive development in Arabidopsis

    Genome Biology 14:R56.

    https://doi.org/10.1186/gb-2013-14-6-r56

    • PubMed
    • Google Scholar
26. 1. Gu Q
    2. Ferrándiz C
    3. Yanofsky MF
    4. Martienssen R

    (1998) The fruitfull mads-box gene mediates cell differentiation during Arabidopsis fruit development

    Development 125:1509–1517.

    https://doi.org/10.1242/dev.125.8.1509

    • PubMed
    • Google Scholar
27. 1. Hartmann U
    2. Höhmann S
    3. Nettesheim K
    4. Wisman E
    5. Saedler H
    6. Huijser P

    (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis

    The Plant Journal 21:351–360.

    https://doi.org/10.1046/j.1365-313x.2000.00682.x

    • PubMed
    • Google Scholar
28. 1. Hofberger JA
    2. Zhou B
    3. Tang H
    4. Jones JDG
    5. Schranz ME

    (2014) A novel approach for multi-domain and multi-gene family identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants

    BMC Genomics 15:966.

    https://doi.org/10.1186/1471-2164-15-966

    • PubMed
    • Google Scholar
29. 1. Hong L
    2. Rumei X

    (1993) Studies on honeydew excretion by greenhouse whitefly, Trialeurodes vaporariorum (Westw.) on its host plant, Cucumis sativus

    Journal of Applied Entomology 115:43–51.

    https://doi.org/10.1111/j.1439-0418.1993.tb00362.x

    • Google Scholar
30. 1. Honma T
    2. Goto K

    (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs

    Nature 409:525–529.

    https://doi.org/10.1038/35054083

    • PubMed
    • Google Scholar
31. 1. Hrabak EM
    2. Chan CWM
    3. Gribskov M
    4. Harper JF
    5. Choi JH
    6. Halford N
    7. Kudla J
    8. Luan S
    9. Nimmo HG
    10. Sussman MR
    11. Thomas M
    12. Walker-Simmons K
    13. Zhu JK
    14. Harmon AC

    (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases

    Plant Physiology 132:666–680.

    https://doi.org/10.1104/pp.102.011999

    • PubMed
    • Google Scholar
32. 1. Huang W
    2. Reyes-Caldas P
    3. Mann M
    4. Seifbarghi S
    5. Kahn A
    6. Almeida RPP
    7. Béven L
    8. Heck M
    9. Hogenhout SA
    10. Coaker G

    (2020) Bacterial vector-borne plant diseases: unanswered questions and future directions

    Molecular Plant 13:1379–1393.

    https://doi.org/10.1016/j.molp.2020.08.010

    • PubMed
    • Google Scholar
33. 1. Huang W
    2. MacLean AM
    3. Sugio A
    4. Maqbool A
    5. Busscher M
    6. Cho ST
    7. Kamoun S
    8. Kuo CH
    9. Immink RGH
    10. Hogenhout SA

    (2021) Parasitic modulation of host development by ubiquitin-independent protein degradation

    Cell 184:5201–5214.

    https://doi.org/10.1016/j.cell.2021.08.029

    • PubMed
    • Google Scholar
34. Preprint

    1. Huang W
    2. Hogenhout SA

    (2022) Interfering with Plant Developmental Timing Promotes Susceptibility to Insect Vectors of a Bacterial Parasite

    bioRxiv.

    https://doi.org/10.1101/2022.03.30.486463

    • Google Scholar
35. 1. Hunter P

    (2018) The revival of the extended phenotype

    EMBO Reports 19:e46477.

    https://doi.org/10.15252/embr.201846477

    • Google Scholar
36. 1. Immink RGH
    2. Gadella TWJ
    3. Ferrario S
    4. Busscher M
    5. Angenent GC

    (2002) Analysis of MADS box protein-protein interactions in living plant cells

    PNAS 99:2416–2421.

    https://doi.org/10.1073/pnas.042677699

    • PubMed
    • Google Scholar
37. 1. Immink RGH
    2. Posé D
    3. Ferrario S
    4. Ott F
    5. Kaufmann K
    6. Valentim FL
    7. de Folter S
    8. van der Wal F
    9. van Dijk ADJ
    10. Schmid M
    11. Angenent GC

    (2012) Characterization of SOC1’s central role in flowering by the identification of its upstream and downstream regulators

    Plant Physiology 160:433–449.

    https://doi.org/10.1104/pp.112.202614

    • PubMed
    • Google Scholar
38. 1. Jonak C
    2. Okrész L
    3. Bögre L
    4. Hirt H

    (2002) Complexity, cross talk and integration of plant MAP kinase signalling

    Current Opinion in Plant Biology 5:415–424.

    https://doi.org/10.1016/s1369-5266(02)00285-6

    • PubMed
    • Google Scholar
39. 1. Katsuma S
    2. Hirota K
    3. Matsuda-Imai N
    4. Fukui T
    5. Muro T
    6. Nishino K
    7. Kosako H
    8. Shoji K
    9. Takanashi H
    10. Fujii T
    11. Arimura S-I
    12. Kiuchi T

    (2022) A Wolbachia factor for male killing in lepidopteran insects

    Nature Communications 13:6764.

    https://doi.org/10.1038/s41467-022-34488-y

    • PubMed
    • Google Scholar
40. 1. Kitazawa Y
    2. Iwabuchi N
    3. Maejima K
    4. Sasano M
    5. Matsumoto O
    6. Koinuma H
    7. Tokuda R
    8. Suzuki M
    9. Oshima K
    10. Namba S
    11. Yamaji Y

    (2022) A phytoplasma effector acts as A ubiquitin-like mediator between floral MADS-box proteins and proteasome shuttle proteins

    The Plant Cell 34:1709–1723.

    https://doi.org/10.1093/plcell/koac062

    • PubMed
    • Google Scholar
41. 1. Kroj T
    2. Chanclud E
    3. Michel-Romiti C
    4. Grand X
    5. Morel JB

    (2016) Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread

    The New Phytologist 210:618–626.

    https://doi.org/10.1111/nph.13869

    • PubMed
    • Google Scholar
42. Website

    1. Krueger F

    (2012) Trim Galore: a wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files, with some extra functionality for MspI-digested RRBS-type (Reduced Representation Bisufite-Seq) libraries

    Accessed April 28, 2016.

    https://www.bioinformatics.babraham.ac.uk/projects/trim_galore/
43. 1. Kumari S
    2. Nagendran K
    3. Rai AB
    4. Singh B
    5. Rao GP
    6. Bertaccini A

    (2019) Global status of phytoplasma diseases in vegetable crops

    Frontiers in Microbiology 10:1349.

    https://doi.org/10.3389/fmicb.2019.01349

    • PubMed
    • Google Scholar
44. 1. Lee IM
    2. Davis RE
    3. Gundersen-Rindal DE

    (2000) Phytoplasma: phytopathogenic mollicutes

    Annual Review of Microbiology 54:221–255.

    https://doi.org/10.1146/annurev.micro.54.1.221

    • PubMed
    • Google Scholar
45. 1. Li Z
    2. Zeng S
    3. Li Y
    4. Li M
    5. Souer E

    (2016) Leaf-like sepals induced by ectopic expression of a SHORT VEGETATIVE PHASE (SVP)-Like MADS-Box gene from the basal eudicot epimedium sagittatum

    Frontiers in Plant Science 7:1461.

    https://doi.org/10.3389/fpls.2016.01461

    • Google Scholar
46. 1. Li P
    2. Lu YJ
    3. Chen H
    4. Day B

    (2020) The lifecycle of the plant immune system

    Critical Reviews in Plant Sciences 39:72–100.

    https://doi.org/10.1080/07352689.2020.1757829

    • PubMed
    • Google Scholar
47. 1. Little D
    2. Gouhier-Darimont C
    3. Bruessow F
    4. Reymond P

    (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis

    Plant Physiology 143:784–800.

    https://doi.org/10.1104/pp.106.090837

    • PubMed
    • Google Scholar
48. 1. Liu X
    2. Sun Z
    3. Dong W
    4. Wang Z
    5. Zhang L

    (2018) Expansion and Functional Divergence of the SHORT VEGETATIVE PHASE (SVP) Genes in Eudicots

    Genome Biology and Evolution 10:3026–3037.

    https://doi.org/10.1093/gbe/evy235

    • PubMed
    • Google Scholar
49. 1. Liu Q
    2. Maqbool A
    3. Mirkin FG
    4. Singh Y
    5. Stevenson CEM
    6. Lawson DM
    7. Kamoun S
    8. Huang W
    9. Hogenhout SA

    (2023) Bimodular architecture of bacterial effector SAP05 that drives ubiquitin-independent targeted protein degradation

    PNAS 120:e2310664120.

    https://doi.org/10.1073/pnas.2310664120

    • PubMed
    • Google Scholar
50. 1. Love MI
    2. Huber W
    3. Anders S

    (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

    Genome Biology 15:550.

    https://doi.org/10.1186/s13059-014-0550-8

    • PubMed
    • Google Scholar
51. 1. Lu YT
    2. Li MY
    3. Cheng KT
    4. Tan CM
    5. Su LW
    6. Lin WY
    7. Shih HT
    8. Chiou TJ
    9. Yang JY

    (2014) Transgenic plants that express the phytoplasma effector SAP11 show altered phosphate starvation and defense responses

    Plant Physiology 164:1456–1469.

    https://doi.org/10.1104/pp.113.229740

    • PubMed
    • Google Scholar
52. 1. Lutz U
    2. Posé D
    3. Pfeifer M
    4. Gundlach H
    5. Hagmann J
    6. Wang C
    7. Weigel D
    8. Mayer KFX
    9. Schmid M
    10. Schwechheimer C

    (2015) Modulation of ambient temperature-dependent flowering in Arabidopsis thaliana by natural variation of flowering locus m

    PLOS Genetics 11:e1005588.

    https://doi.org/10.1371/journal.pgen.1005588

    • PubMed
    • Google Scholar
53. 1. MacLean AM
    2. Sugio A
    3. Makarova OV
    4. Findlay KC
    5. Grieve VM
    6. Tóth R
    7. Nicolaisen M
    8. Hogenhout SA

    (2011) Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants

    Plant Physiology 157:831–841.

    https://doi.org/10.1104/pp.111.181586

    • PubMed
    • Google Scholar
54. 1. MacLean AM
    2. Orlovskis Z
    3. Kowitwanich K
    4. Zdziarska AM
    5. Angenent GC
    6. Immink RGH
    7. Hogenhout SA

    (2014) Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner

    PLOS Biology 12:e1001835.

    https://doi.org/10.1371/journal.pbio.1001835

    • PubMed
    • Google Scholar
55. 1. Mateos JL
    2. Madrigal P
    3. Tsuda K
    4. Rawat V
    5. Richter R
    6. Romera-Branchat M
    7. Fornara F
    8. Schneeberger K
    9. Krajewski P
    10. Coupland G

    (2015) Combinatorial activities of SHORT VEGETATIVE PHASE and FLOWERING LOCUS C define distinct modes of FLOWERING regulation in Arabidopsis

    Genome Biology 16:31.

    https://doi.org/10.1186/s13059-015-0597-1

    • PubMed
    • Google Scholar
56. 1. Mayer CJ
    2. Vilcinskas A
    3. Gross J

    (2008a) Phytopathogen lures its insect vector by altering host plant odor

    Journal of Chemical Ecology 34:1045–1049.

    https://doi.org/10.1007/s10886-008-9516-1

    • PubMed
    • Google Scholar
57. 1. Mayer CJ
    2. Vilcinskas A
    3. Gross J

    (2008b) Pathogen-induced release of plant allomone manipulates vector insect behavior

    Journal of Chemical Ecology 34:1518–1522.

    https://doi.org/10.1007/s10886-008-9564-6

    • PubMed
    • Google Scholar
58. 1. Miao YT
    2. Deng Y
    3. Jia HK
    4. Liu YD
    5. Hou ML

    (2018) Proteomic analysis of watery saliva secreted by white-backed planthopper, Sogatella furcifera

    PLOS ONE 13:e0193831.

    https://doi.org/10.1371/journal.pone.0193831

    • PubMed
    • Google Scholar
59. 1. Nørgaard LS
    2. Phillips BL
    3. Hall MD

    (2019) Can pathogens optimize both transmission and dispersal by exploiting sexual dimorphism in their hosts?

    Biology Letters 15:20190180.

    https://doi.org/10.1098/rsbl.2019.0180

    • PubMed
    • Google Scholar
60. 1. Orlovskis Z
    2. Hogenhout SA

    (2016) A bacterial parasite effector mediates insect vector attraction in host plants independently of developmental changes

    Frontiers in Plant Science 7:885.

    https://doi.org/10.3389/fpls.2016.00885

    • PubMed
    • Google Scholar
61. 1. Pecher P
    2. Moro G
    3. Canale MC
    4. Capdevielle S
    5. Singh A
    6. MacLean A
    7. Sugio A
    8. Kuo CH
    9. Lopes JRS
    10. Hogenhout SA

    (2019) Phytoplasma SAP11 effector destabilization of TCP transcription factors differentially impact development and defence of Arabidopsis versus maize

    PLOS Pathogens 15:e1008035.

    https://doi.org/10.1371/journal.ppat.1008035

    • PubMed
    • Google Scholar
62. 1. Pertea M
    2. Kim D
    3. Pertea GM
    4. Leek JT
    5. Salzberg SL

    (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown

    Nature Protocols 11:1650–1667.

    https://doi.org/10.1038/nprot.2016.095

    • PubMed
    • Google Scholar
63. 1. Rid M
    2. Mesca C
    3. Ayasse M
    4. Gross J

    (2016) Apple proliferation phytoplasma influences the pattern of plant volatiles emitted depending on pathogen virulence

    Frontiers in Ecology and Evolution 3:152.

    https://doi.org/10.3389/fevo.2015.00152

    • Google Scholar
64. 1. Roy BA

    (1993) Floral mimicry by a plant pathogen

    Nature 362:56–58.

    https://doi.org/10.1038/362056a0

    • Google Scholar
65. 1. Sarris PF
    2. Cevik V
    3. Dagdas G
    4. Jones JDG
    5. Krasileva KV

    (2016) Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens

    BMC Biology 14:8.

    https://doi.org/10.1186/s12915-016-0228-7

    • PubMed
    • Google Scholar
66. 1. Serbus LR
    2. Casper-Lindley C
    3. Landmann F
    4. Sullivan W

    (2008) The genetics and cell biology of Wolbachia-host interactions

    Annual Review of Genetics 42:683–707.

    https://doi.org/10.1146/annurev.genet.41.110306.130354

    • PubMed
    • Google Scholar
67. 1. Shen L
    2. Thong Z
    3. Gong X
    4. Shen Q
    5. Gan Y
    6. Yu H

    (2014) The putative PRC1 RING-finger protein AtRING1A regulates FLOWERING through repressing MADS AFFECTING FLOWERING genes in Arabidopsis

    Development 141:1303–1312.

    https://doi.org/10.1242/dev.104513

    • PubMed
    • Google Scholar
68. 1. Shiu SH
    2. Bleecker AB

    (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases

    PNAS 98:10763–10768.

    https://doi.org/10.1073/pnas.181141598

    • PubMed
    • Google Scholar
69. 1. Snoeck S
    2. Guayazán-Palacios N
    3. Steinbrenner AD

    (2022) Molecular tug-of-war: Plant immune recognition of herbivory

    The Plant Cell 34:1497–1513.

    https://doi.org/10.1093/plcell/koac009

    • PubMed
    • Google Scholar
70. 1. Stahl E
    2. Brillatz T
    3. Ferreira Queiroz E
    4. Marcourt L
    5. Schmiesing A
    6. Hilfiker O
    7. Riezman I
    8. Riezman H
    9. Wolfender JL
    10. Reymond P

    (2020) Phosphatidylcholines from Pieris brassicae eggs activate an immune response in Arabidopsis

    eLife 9:e60293.

    https://doi.org/10.7554/eLife.60293

    • PubMed
    • Google Scholar
71. 1. Sugio A
    2. Kingdom HN
    3. MacLean AM
    4. Grieve VM
    5. Hogenhout SA

    (2011a) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis

    PNAS 108:E1254–E1263.

    https://doi.org/10.1073/pnas.1105664108

    • PubMed
    • Google Scholar
72. 1. Sugio A
    2. MacLean AM
    3. Kingdom HN
    4. Grieve VM
    5. Manimekalai R
    6. Hogenhout SA

    (2011b) Diverse targets of phytoplasma effectors: from plant development to defense against insects

    Annual Review of Phytopathology 49:175–195.

    https://doi.org/10.1146/annurev-phyto-072910-095323

    • PubMed
    • Google Scholar
73. 1. Sugio A
    2. MacLean AM
    3. Hogenhout SA

    (2014) The small phytoplasma virulence effector SAP11 contains distinct domains required for nuclear targeting and CIN-TCP binding and destabilization

    The New Phytologist 202:838–848.

    https://doi.org/10.1111/nph.12721

    • PubMed
    • Google Scholar
74. 1. Sun LM
    2. Zhang JZ
    3. Hu CG

    (2016) Characterization and Expression Analysis of PtAGL24, a SHORT VEGETATIVE PHASE/AGAMOUS-LIKE 24 (SVP/AGL24)-Type MADS-Box Gene from Trifoliate Orange (Poncirus trifoliata L. Raf.)

    Frontiers in Plant Science 7:823.

    https://doi.org/10.3389/fpls.2016.00823

    • PubMed
    • Google Scholar
75. 1. Suzuki M
    2. Kitazawa Y
    3. Iwabuchi N
    4. Maejima K
    5. Matsuyama J
    6. Matsumoto O
    7. Oshima K
    8. Namba S
    9. Yamaji Y

    (2024) Target degradation specificity of phytoplasma effector phyllogen is regulated by the recruitment of host proteasome shuttle protein

    Molecular Plant Pathology 25:e13410.

    https://doi.org/10.1111/mpp.13410

    • PubMed
    • Google Scholar
76. 1. Tan CM
    2. Li C-H
    3. Tsao N-W
    4. Su L-W
    5. Lu Y-T
    6. Chang SH
    7. Lin YY
    8. Liou J-C
    9. Hsieh L-C
    10. Yu J-Z
    11. Sheue C-R
    12. Wang S-Y
    13. Lee C-F
    14. Yang J-Y

    (2016) Phytoplasma SAP11 alters 3-isobutyl-2-methoxypyrazine biosynthesis in Nicotiana benthamiana by suppressing NbOMT1

    Journal of Experimental Botany 67:4415–4425.

    https://doi.org/10.1093/jxb/erw225

    • Google Scholar
77. 1. Thimm O
    2. Bläsing O
    3. Gibon Y
    4. Nagel A
    5. Meyer S
    6. Krüger P
    7. Selbig J
    8. Müller LA
    9. Rhee SY
    10. Stitt M

    (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes

    The Plant Journal 37:914–939.

    https://doi.org/10.1111/j.1365-313x.2004.02016.x

    • PubMed
    • Google Scholar
78. 1. Tomkins M
    2. Kliot A
    3. Marée AF
    4. Hogenhout SA

    (2018) A multi-layered mechanistic modelling approach to understand how effector genes extend beyond phytoplasma to modulate plant hosts, insect vectors and the environment

    Current Opinion in Plant Biology 44:39–48.

    https://doi.org/10.1016/j.pbi.2018.02.002

    • PubMed
    • Google Scholar
79. 1. Tong WH
    2. Pavey C
    3. O’Handley R
    4. Vyas A

    (2021) Behavioral biology of Toxoplasma gondii infection

    Parasites & Vectors 14:77.

    https://doi.org/10.1186/s13071-020-04528-x

    • Google Scholar
80. 1. Usadel B
    2. Nagel A
    3. Thimm O
    4. Redestig H
    5. Blaesing OE
    6. Palacios-Rojas N
    7. Selbig J
    8. Hannemann J
    9. Piques MC
    10. Steinhauser D
    11. Scheible W-R
    12. Gibon Y
    13. Morcuende R
    14. Weicht D
    15. Meyer S
    16. Stitt M

    (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses

    Plant Physiology 138:1195–1204.

    https://doi.org/10.1104/pp.105.060459

    • PubMed
    • Google Scholar
81. 1. Usadel B
    2. Poree F
    3. Nagel A
    4. Lohse M
    5. Czedik‐eysenberg A
    6. Stitt M

    (2009) A guide to using MapMan to visualize and compare Omics data in plants: A case study in the crop species, Maize

    Plant, Cell & Environment 32:1211–1229.

    https://doi.org/10.1111/j.1365-3040.2009.01978.x

    • Google Scholar
82. Book

    1. van Verk M

    (2010)

    WRKY Transcription Factors Involved in Salicylic Acid-Induced Defense Gene Expression

    Universiteit Leiden.

    • Google Scholar
83. 1. Wang R
    2. Bai B
    3. Li D
    4. Wang J
    5. Huang W
    6. Wu Y
    7. Zhao L

    (2024) Phytoplasma: A plant pathogen that cannot be ignored in agricultural production-Research progress and outlook

    Molecular Plant Pathology 25:e13437.

    https://doi.org/10.1111/mpp.13437

    • PubMed
    • Google Scholar
84. 1. Weintraub PG
    2. Beanland L

    (2006) Insect vectors of phytoplasmas

    Annual Review of Entomology 51:91–111.

    https://doi.org/10.1146/annurev.ento.51.110104.151039

    • PubMed
    • Google Scholar
85. 1. Wilson DC
    2. Kempthorne CJ
    3. Carella P
    4. Liscombe DK
    5. Cameron RK

    (2017) Age-Related Resistance in Arabidopsis thaliana Involves the MADS-Domain Transcription Factor SHORT VEGETATIVE PHASE and Direct Action of Salicylic Acid on Pseudomonas syringae

    Molecular Plant-Microbe Interactions 30:919–929.

    https://doi.org/10.1094/MPMI-07-17-0172-R

    • PubMed
    • Google Scholar
86. 1. Wu R
    2. Tomes S
    3. Karunairetnam S
    4. Tustin SD
    5. Hellens RP
    6. Allan AC
    7. Macknight RC
    8. Varkonyi-Gasic E

    (2017) SVP-like MADS box genes control dormancy and budbreak in apple

    Frontiers in Plant Science 8:477.

    https://doi.org/10.3389/fpls.2017.00477

    • PubMed
    • Google Scholar
87. 1. Yan X
    2. Yuan X
    3. Lv J
    4. Zhang B
    5. Huang Y
    6. Li Q
    7. Ma J
    8. Li Y
    9. Wang X
    10. Li Y
    11. Yu Y
    12. Liu Q
    13. Liu T
    14. Mi W
    15. Dong C

    (2024) Molecular basis of SAP05-mediated ubiquitin-independent proteasomal degradation of transcription factors

    Nature Communications 15:1170.

    https://doi.org/10.1038/s41467-024-45521-7

    • PubMed
    • Google Scholar
88. 1. Yang CY
    2. Huang YH
    3. Lin CP
    4. Lin YY
    5. Hsu HC
    6. Wang CN
    7. Liu LYD
    8. Shen BN
    9. Lin SS

    (2015) MicroRNA396-Targeted SHORT VEGETATIVE PHASE Is required to repress flowering and is related to the development of abnormal flower symptoms by the phyllody symptoms1 effector

    Plant Physiology 168:1702–1716.

    https://doi.org/10.1104/pp.15.00307

    • PubMed
    • Google Scholar
89. 1. Yoo SD
    2. Cho YH
    3. Sheen J

    (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis

    Nature Protocols 2:1565–1572.

    https://doi.org/10.1038/nprot.2007.199

    • PubMed
    • Google Scholar
90. 1. Zhang L
    2. Du Y
    3. Qu Q
    4. Zheng Q

    (2024) Structure basis for recognition of plant Rpn10 by phytoplasma SAP05 in ubiquitin-independent protein degradation

    iScience 27:108892.

    https://doi.org/10.1016/j.isci.2024.108892

    • PubMed
    • Google Scholar
91. 1. Zheng Y
    2. Ren N
    3. Wang H
    4. Stromberg AJ
    5. Perry SE

    (2009) Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15

    The Plant Cell 21:2563–2577.

    https://doi.org/10.1105/tpc.109.068890

    • PubMed
    • Google Scholar

Author details

1. Zigmunds Orlovskis

   John Innes Centre, Norwich Research Park, Norwich, United Kingdom

   Present address

   Latvian Biomedical Research and Study Centre, Rātsupītes 1k-1, Rīga, Latvia

   Contribution

   Conceptualization, Data curation, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   zigmunds.orlovskis@biomed.lu.lv

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8583-9814

2. Archana Singh

   John Innes Centre, Norwich Research Park, Norwich, United Kingdom

   Present address

   Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, United Kingdom

   Contribution

   Data curation, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5027-4582

3. Adi Kliot

   John Innes Centre, Norwich Research Park, Norwich, United Kingdom

   Present address

   Department of Entomology, ARO, the Volcani Center, HaMaccabim Road 68, 14 PO Box 15159, Rishon LeZion, Israel

   Contribution

   Validation, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0370-0817

4. Weijie Huang

   John Innes Centre, Norwich Research Park, Norwich, United Kingdom

   Contribution

   Investigation, Visualization, Writing – review and editing

   Competing interests

   No competing interests declared

5. Saskia A Hogenhout

   John Innes Centre, Norwich Research Park, Norwich, United Kingdom

   Contribution

   Conceptualization, Formal analysis, Supervision, Funding acquisition, Validation, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   saskia.hogenhout@jic.ac.uk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1371-5606

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