The phytopathogen ‘Candidatus Phytoplasma mali’ alters apple tree phloem composition and affects oviposition behavior of its vector Cacopsylla picta

Abstract

Apple proliferation disease is caused by the phloem-dwelling bacterium ‘Candidatus Phytoplasma mali’, inducing morphological changes in its host plant apple, such as witches’ broom formation. Furthermore, it triggers physiological alterations like emission of volatile organic compounds or phytohormone levels in the plant. In our study, we assessed phytoplasma-induced changes in the phloem by sampling phloem sap from infected and non-infected apple plants. In infected plants, the soluble sugar content increased and the composition of phloem metabolites differed significantly between non-infected and infected plants. Sugar and sugar alcohol levels increased in diseased plants, while organic and amino acid content remained constant. As ‘Ca. P. mali’ is vectored by the phloem-feeding insect Cacopsylla picta (Foerster, 1848), we assessed whether the insect–plant interaction was affected by ‘Ca. P. mali’ infection of the common host plant Malus domestica Borkh. Binary-choice oviposition bioassays between infected and non-infected apple leaves revealed C. picta’s preference for non-infected leaves. It is assumed and discussed that the changes in vector behavior are attributable to plant-mediated effects of the phytoplasma infection.

Involvement of SUT1 and SUT2 Sugar Transporters in the Impairment of Sugar Transport and Changes in Phloem Exudate Contents in Phytoplasma-Infected Plants

“…Interestingly, our data indicates that the infection did not affect the malate contents in phloem sap-enriched exudates. They differ from other reports of higher accumulations in malate reported in the sap and in the main veins of infected plants [ 25 , 33 , 36 ]. Interestingly, malate accumulates in the apoplasm [ 77 , 78 ].…”

“…Studies on symptomatic, well-established phytoplasma infections reported disorganization of the vascular tissues [ 4 , 31 ] and the transcriptional reprogramming of genes involved in sugar transport and metabolism [ 16 , 18 , 24 , 28 , 32 , 33 ]. A phytoplasma infection also triggers modifications in the phloem sap composition [ 25 , 34 , 35 , 36 ], with changes in metabolites produced by diverse metabolic pathways. Such effects could be triggered by the phytoplasma for nutrition, plant defense response or physiological adjustments of impaired phloem activity [ 5 ].…”

Specialized 16SrX phytoplasmas induce diverse morphological and physiological changes in their respective fruit crops

“…In contrast, the soluble sugar content increased and the composition of phloem metabolites differed significantly between Ca . P. mali infected and non-infected apple plants [ 35 ]. Furthermore, sugar and sugar alcohol levels increased in diseased plants, while organic and amino acid content remained constant.…”

“…Therefore, morphological changes of the plant vascular system may affect psyllid feeding behaviour and suitability of plants as hosts of vector insects. Additionally, phloem/xylem components may influence host choice and oviposition behaviour of psyllids [ 31 , 32 , 34 , 35 ]. To detect appropriate host plants for feeding and reproduction, volatile signals are used by many vectoring psyllid species during migration [ 36 – 43 ].…”

Behavior Matters—Future Need for Insect Studies on Odor-Mediated Host Plant Recognition with the Aim of Making Use of Allelochemicals for Plant Protection

“…whereas the decision to lay eggs needed gustatory stimuli from non-volatile chemical signals located in the phloem tissue 55. …”