Sugio, A. | Search bioRxiv

bioRxiv2022

Pea-adapted biotype of the aphid Acyrthosiphon pisum induces susceptibility of pea to non-adapted biotype enabling improved feeding and performance

Most insect herbivores are adapted to feed on a few host plants only, but the mechanisms underlying plant specialization are poorly understood. One of the dominant hypotheses is that insects inject an oral secretion into the plant that manipulates the plants defences resulting in induced susceptibility. We tested this hypothesis on the pea aphid (Acyrthosiphon pisum), which forms multiple biotypes, each specialized on specific legume hosts. In particular, we tested whether a pea-adapted biotype can induce host susceptibility on pea, which should positively affect the fitness of a non-pea-adapted biotype. We found that survival and fecundity of an alfalfa-adapted biotype on pea were enhanced by co-infestation but not pre-infestation with a pea-adapted biotype. The electrical penetration graph (EPG) method was then used to dissect the components of alfalfa biotype feeding behaviour on pea with and without co-infestation by the pea biotype. While probing time did not differ between these two conditions, differences were observed in most other EPG parameters. When co-infested with the pea-adapted biotype, the alfalfa-adapted biotype was more likely to establish a phloem feeding and exhibited a longer ingestion time on pea. Our results clearly indicated that the pea-adapted biotype induced pea susceptibility by increasing the accessibility of non-pea-adapted aphids to the host phloem sap, and as a result, the alfalfa biotype increased its survival rate and fecundity. These results contribute to understanding how aphids manipulate their specific host plants.

ecology↗

bioRxiv2021

Parasite co-opts a ubiquitin receptor to induce a plethora of developmental changes

Obligate parasites can induce complex and substantial phenotypic changes in their hosts in ways that favour their transmission to other trophic levels. However, mechanisms underlying these changes remain largely unknown. Here, we demonstrate how SAP05 protein effectors from insect-vectored plant pathogenic phytoplasmas take control of several plant developmental processes to simultaneously prolong host lifespan and induce witchs broom-like proliferations of leaf and sterile shoots, organs colonized by phytoplasmas and vectors. SAP05 acts by mediating the concurrent degradation of SPL and GATA developmental regulators via a process that uniquely relies on hijacking the plant ubiquitin receptor RPN10 independently of substrate lysine ubiquitination. RPN10 is highly conserved among eukaryotes, but SAP05 does not bind insect vector RPN10. A two-amino-acid substitution within plant RPN10 generates a functional variant that is resistant to SAP05 activities. Therefore, one effector protein enables obligate parasitic phytoplasmas to induce a plethora of developmental phenotypes in their hosts.

molecular biology↗

bioRxiv2019

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

Phytoplasmas are insect-transmitted bacterial pathogens that colonize a wide range of plant species, including vegetable and cereal crops, and herbaceous and woody ornamentals. Phytoplasma-infected plants often show dramatic symptoms, including proliferation of shoots (witchs brooms), changes in leaf shapes and production of green sterile flowers (phyllody). Aster Yellows phytoplasma Witches Broom (AY-WB) infects dicots and its effector, secreted AYWB protein 11 (SAP11), was shown to be responsible for the induction of shoot proliferation and leaf shape changes of plants. SAP11 acts by destabilizing TEOSINTE BRANCHED 1-CYCLOIDEA-PROLIFERATING CELL FACTOR (TCP) transcription factors, particularly the class II TCPs of the CYCLOIDEA/TEOSINTE BRANCHED 1 (CYC/TB1) and CINCINNATA (CIN)-TCP clades. SAP11 homologs are also present in phytoplasmas that cause economic yield losses in monocot crops, such as maize, wheat and coconut. Here we show that a SAP11 homolog of Maize Bushy Stunt Phytoplasma (MBSP), which has a range primarily restricted to maize, destabilizes only TB1/CYC TCPs. SAP11MBSP and SAP11AYWB both induce axillary branching and SAP11AYWB also alters leaf development of Arabidopsis thaliana and maize. However, only in maize, SAP11MBSP prevents female inflorescence development, phenocopying maize tb1 lines, whereas SAP11AYWB prevents male inflorescence development and induces feminization of tassels. SAP11AYWB promotes fecundity of the AY-WB leafhopper vector on A. thaliana and modulates the expression of A. thaliana leaf defence response genes that are induced by this leafhopper, in contrast to SAP11MBSP. Neither of the SAP11 effectors promote fecundity of AY-WB and MBSP leafhopper vectors on maize. These data provide evidence that class II TCPs have overlapping but also distinct roles in regulating development and defence in a dicot and a monocot plant species that is likely to shape SAP11 effector evolution depending on the phytoplasma host range.\n\nAuthor summaryPhytoplasmas are parasites of a wide range of plant species and are transmitted by sap-feeding insects, such as leafhoppers. Phytoplasma-infected plants are often easily recognized because of their dramatic symptoms, including shoot proliferations (witchs brooms) and altered leaf shapes, leading to severe economic losses of crops, ornamentals and trees worldwide. We previously found that the virulence protein SAP11 of aster yellows witches broom phytoplasma (AY-WB) interferes with a specific group of plant transcription factors, named TCPs, leading to witches brooms and leaf shape changes of the model plant Arabidopsis thaliana. SAP11 has been characterized in a number of other phytoplasmas. However, it is not known how phytoplasmas and their SAP11 proteins modulate processes in crops, including cereals such as maize. We identified a SAP11 homolog in Maize bushy stunt phytoplasma (MBSP), a pathogen that can cause severe yield losses of maize. We found that SAP11 interactions with TCPs are conserved between maize and Arabidopsis, and that MBSP SAP11 interferes with less TCPs compared to AY-WB SAP11. This work provides new insights into how phytoplasmas change maize architecture and corn production. Moreover, we found that TCPs regulate leaf defence responses to phytoplasma leafhopper vectors in Arabidopsis, but not in maize.

evolutionary biology↗