A galling insect activates plant reproductive programs during gall development

Abstract

Many insect species have acquired the ability to redirect plant development to form unique organs called galls, which provide these insects with unique, enhanced food and protection from enemies and the elements. Many galls resemble flowers or fruits, suggesting that elements of reproductive development may be involved. We tested this hypothesis using RNA sequencing to quantify the transcriptional responses of wild grapevine (Vitis riparia) leaves to a galling parasite, phylloxera (Daktulosphaira vitifoliae). If development of reproductive structures is part of gall formation, we expected to find significantly elevated expression of genes involved in flower and/or fruit development in developing galls as opposed to ungalled leaves. We found that reproductive gene ontology categories were significantly enriched in developing galls, and that expression of many candidate genes involved in floral development were significantly increased, particularly in later gall stages. The patterns of gene expression found in galls suggest that phylloxera exploits vascular cambium to provide meristematic tissue and redirects leaf development towards formation of carpels. The phylloxera leaf gall appears to be phenotypically and transcriptionally similar to the carpel, due to the parasite hijacking underlying genetic machinery in the host plant.

Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development

“…In many galls the vasculature is generated to connect to the source of host plant tissue, and this process is suggested to be regulated by CLE and LRR–RLK genes, together with the other factors such as the auxin–dependent process shown above. A previous study with grapevine gall has shown that CLE44 and WOX4 are up–regulated in galls [13], supporting our hypothesis that these factors are commonly involved in vascular development in galls.…”

“…Shape and color of some galls show similarity to flowers and fruits. From the grapevine gall research, it is suggested that genes involved in reproductive organ development are up–regulated in developing galls [13]. Floral organ identity is determined by combined actions of the floral MADS genes [74–75].…”

“…Transcriptomes of both host plants and gall aphids have helped elucidate the molecular mechanisms of tannin biosynthesis and aphid reproduction, respectively [11–12]. Another example is the gall of wild grapevine ( Vitis riparia ) generated by phylloxera ( Daktulosphaira vitifoliae ), suggesting that pathways of floral organ development and procambium differentiation are involved in gall development [13]. These reports propose the molecular mechanism of interaction between gall insects and host plants, although, the gall structure varies widely making it difficult to identify the fundamental processes of gall development.…”

Cytokinins Are Abundant and Widespread among Insect Species

“…However, the CK concentrations we report are much higher than those used by [62] (~9 pmol/g fwt), and how plants may respond to potentially much higher concentrations of CKs secreted by insects is as yet unknown. Several transcriptomic studies of gall systems report that gene expression in plant defense pathways are either unaffected or down-regulated in galls relative to un-galled plant tissues [19,[114][115][116][117][118][119][120], while other studies make no mention of effects of galling on host defenses or report up-regulation of plant defensive pathways [121][122][123][124][125]. Given the complicated relationships among phytohormones [126], there is likely to be crosstalk between the CK signaling pathway and other plant defense pathways, so perhaps CKs modulate defense.…”

Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp

“…In contrast to microbial systems, gall induction by animals is poorly understood for all but a tiny minority of economically important species, including root knot and cyst nematodes ( Heterodera , Globodera and Meloidogyne species) [18–20], Hessian fly ( Mayetiola destructor ) [21–24] and Phylloxera [25,26]. Nevertheless, with an estimated 30,000 species [27], gall inducing arthropods (and particularly insects) are abundant and ecologically important components of many biological communities [27].…”