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

Abstract

Phytoplasmas are insect-transmitted phytopathogenic bacteria that can alter plant morphology and the longevity and reproduction rates and behavior of their insect vectors. There are various examples of animal and plant parasites that alter the host phenotype to attract insect vectors, but it is unclear how these parasites accomplish this. We hypothesized that phytoplasmas produce effectors that modulate specific targets in their hosts leading to the changes in plant development and insect performance. Previously, we sequenced and mined the genome of Aster Yellows phytoplasma strain Witches' Broom (AY-WB) and identified 56 candidate effectors. Here, we report that the secreted AY-WB protein 11 (SAP11) effector modulates plant defense responses to the advantage of the AY-WB insect vector Macrosteles quadrilineatus. SAP11 binds and destabilizes Arabidopsis CINCINNATA (CIN)-related TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FAC-TORS 1 and 2 (TCP) transcription factors, which control plant development and promote the expression of lipoxygenase (LOX) genes involved in jasmonate (JA) synthesis. Both the Arabidopsis SAP11 lines and AY-WB-infected plants produce less JA on wounding. Furthermore, the AY-WB insect vector produces more offspring on AY-WB-infected plants, SAP11 transgenic lines, and plants impaired in CIN-TCP and JA synthesis. Thus, SAP11-mediated destabilization of CIN-TCPs leads to the down-regulation of LOX2 expression and JA synthesis and an increase in M. quadrilineatus progeny. Phytoplasmas are obligate inhabitants of their plant host and insect vectors, in which the latter transmits AY-WB to a diverse range of plant species. This finding demonstrates that pathogen effectors can reach beyond the pathogen-host interface to modulate a third organism in the biological interaction.Arabidopsis development | insect herbivore | jasmonic acid | symbiosis | Hemiptera

TheArabidopsis thalianaTCP transcription factors: A broadening horizon beyond development

“…Mining genomic sequence data leads to the identification of 56 candidate effector proteins encoded by the genome of the Aster Yellows phytoplasma strain Witches Broom (AY-WB). 65 Of these potential effectors, the secreted AY-WB protein 11 (SAP11) is able to bind and destabilize all of the 8 Arabidopsis CIN-related TCP proteins, 65 which operate redundantly to promote the expression of LOX2 that is involved in JA synthesis. 65 Both SAP11-overexpressing lines and AY-WB-infected Arabidopsis plants accumulate less JA on wounding.…”

“…63 Apart from playing a pivotal role in plant ETI as described above, TCP proteins also participate in defense against insect vectors in phytoplasm-infected plants. 65 Phytoplasms belong to insect-transmitted phytopathogenic bacteria, which can secrete pathogen effectors to modulate specific plant targets, thus resulting in changes in plant development and insect performance. Mining genomic sequence data leads to the identification of 56 candidate effector proteins encoded by the genome of the Aster Yellows phytoplasma strain Witches Broom (AY-WB).…”

“…[98][99][100][101][102][103][104][105] Several recent studies have demonstrated that TCP transcription factors also function as a cellular hub in plant defense signaling. [63][64][65] Based on the systematic analyses of binary protein-protein interactions between Arabidopsis immune proteins, ca. 8000 full-length Arabidopsis proteins and effector proteins of 2 evolutionarily divergent pathogens, including the Gram-negative bacterium Pseudomonas syringae (Psy) and the obligate biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa), a plant-pathogen protein-protein interactome network was created, which contain 1358 interactions among 926 proteins, including 83 pathogen effectors, 170 immune proteins and 673 immune interactors.…”

“…TCP proteins from various species throughout the plant kingdom have been demonstrated to regulate a large variety of biological processes, such as floral asymmetry, 23-34 plant architectures including branching, [35][36][37][38][39] lateral organ development, 40-55 seed germination, 56,57 gametophyte development, 58,59 leaf senescence, 44,60 circadian rhythms, 61,62 and defense responses. [63][64][65] Noteworthily, several aspects of these plant processes involve a regulatory role for TCPs in the biosynthetic pathways of bioactive compounds. 19,60,[66][67][68][69] In this review, developmental functions of TCP proteins are synoptically summarized and their participation in the biosynthetic processes impacting both plant development and defense against leafhoppers are emphasized (Table A1).…”

Identification of Plasmodiophora brassicae effectors — A challenging goal

“…Among these well-characterized biotrophic pathogens are: ( i ) Puccinia monoica [23] which, similar to aster yellows phytoplasma [24], can induce floral mimicry in order to promote its own sexual reproduction; ( ii ) Melampsora lini [25], which produces effector proteins in haustoria that are recognized inside the plant cell [26]; and ( iii ) Cladosporium fulvum , the tomato pathogen which, during infection, secretes the chitin-binding virulence factor Avr4 that is thought to protect the fungal chitin cell wall from hydrolysis by plant produced chitinases [27]. Extensive studies with P. graminis f. sp.…”