A new perspective on plant defense against foliar gall-forming aphids through activation of the fruit abscission pathway

Abstract

The peach aphid Tuberocephalus momonis seriously damages leaves and forms galls in the peach species Prunus persica f. rubro-plena, P. persica, and P. davidiana. Leaves bearing galls formed by these aphids will be abscised at least two months earlier than the healthy leaves on the same tree. Thus, we hypothesize that gall development is likely to be governed by phytohormones involved in normal organogenesis. The soluble sugar content was positively correlated between gall tissues and fruits, suggesting that the galls are sink organs. The results of UPLC-MS/MS analysis showed that higher concentrations of 6-benzylaminopurine (BAP) accumulated in both the gall-forming aphids, the galls themselves and the fruits of peach species than in healthy leaves, suggesting that BAP was being synthesized by the insects to stimulate the establishment of a gall. A significant increase in the concentrations of abscisic acid (ABA) in fruits and jasmonic acid (JA) in gall tissues indicated that these plants are defending from the galls. The concentrations of 1-amino-cyclopropane-1-carboxylic acid (ACC) significantly increased in gall tissues compared with healthy leaves, and were positively correlated with both fruit and gall development. In addition, transcriptome sequencing analysis revealed that during gall abscission, differentially expressed genes in both 'ETR-SIMKK-ERE1' and 'ABA-PYR/PYL/RCAR-PP2C-SnRK2' were significantly enriched during gall abscission. Our results showed that ethylene pathway was involved in the abscission of gall, and this gall abscission allowed the host plants to protect themselves from the gall-forming insects, at least partially.