Phytohormone profiling reveals fungal signatures and strong manipulation of infection cycle in theGymnosporangium juniper-virginianaedual-host plant system

Abstract

The aim of this work was to examine the function of phytohormones in the pathogenesis of cedar-apple rust, a fungal disease caused by Gymnosporangium juniper-virginianae Schwein. on Eastern red cedar (Juniperus virginiana L.) and crabapple trees (Malus spp. Mill.). Control cedar branchlets, gall tissues, fungal telial horns, as well as healthy and infected apple leaves were collected throughout fungal and plant development and used for profiling endogenous cytokinins (CK) and abscisic acid (ABA) by high performance liquid chromatography – electrospray ionization – tandem mass spectrometry. Phytohormone composition implicates cytokinin involvement in the development of rust infection. Moreover, increased levels of total CKs, as well as the unique profiles of sporulating galls on cedar trees, telial horns, and infected apple leaves, dominated by cis-Zeatin type CK, suggest that the fungus can synthesize hormones to facilitate the infection process. Distribution of ABA in the fungal and plant tissues indicates an important function of this stress hormone in regulating rapid changes in osmotic pressure during teliospore production by the galls. This study of the cedar-apple rust disease cycle is the first elucidation of phytohormones profiling between a pathogenic fungus and the attacked plant in a dual-host infection system.

The Origins and Roles of Methylthiolated Cytokinins: Evidence From Among Life Kingdoms

“…The dominance of c Z- and iP-type CKs in the hormone profiles of saprophytic and biotrophic fungal species suggests that the tRNA degradation is the predominant CK pathway in that kingdom ( Morrison et al, 2015b ; Moffatt et al, 2018 ). A fungal tRNA-isopentenyltransferase gene homolog ( MOD5 ) was first identified in yeast ( Saccharomyces cerevisiae ) ( Laten et al, 1978 ; Dihanich et al, 1987 ).…”

Comparative transcriptome analysis of juniper branches infected by Gymnosporangium spp. highlights their different infection strategies associated with cytokinins

“…While it is unclear whether there is rust-derived cis-zeatin. A recent study confirmed that cis-zeatin was detected in G. juniper-virginianae induced gall tissues as well as the wet telia, but not in control cedar branchlets [ 33 ]. To verify the effect of G. yamadae derived CKs on the induction of galls, we firstly examined the CKs content in juniper and G. yamadae , and found that galls and the telia contained significantly higher concentrations of CKs than the control sample (Fig.…”

“…Subsequently, along with G. yamadae teliospores development and maturity, vesicular transport-related genes and additional starch and sucrose synthesis-related genes were up-regulated at the middle stage (II_GY_J) and numbers of energy metabolism-related genes were up-regulated in the late stage (III_GY_J), which suggested a general function of galls as a carbohydrate source for the growth of G. yamadae teliospores. Correspondingly, rapid changes in the water and nutrient content in the gall lead to an increase in osmotic pressure, which induces the expression of ABA synthesis-related genes and an increase in ABA content, especially during the formation of large numbers of teliospores (II_GY_J) [ 33 , 52 ]. Besides, genes involved in auxin signaling transduction pathway were also specifically up-regulated in II_GY_J, which possibly contributed to teliospores germination [ 20 , 53 , 54 ].…”

“…The bottom line is that these organisms that provoke plant tissue proliferation are all dependent on living plants, which may reflect the common survival strategies of these parasites or symbiotic organisms. Rust fungi can induce malformation, swelling and even galls on plant hosts, the symptom is relatively more typical in Gymnosporangium species [ 7 , 13 , 33 , 34 ]. In G. juniper - virginianae -cedar pathosystem, the rust fungi synthesized CKs that might facilitate the gall formation [ 33 ], which enlighten us postulate that CKs derived by G. yamadae might be an important factor that causes galls and results in the different symptoms on juniper between G. asiaticum -juniper and G. yamadae -juniper pathosystems.…”

“…Several previous studies have also shown that rust fungi, including Puccinia recondita f. sp. tritici [ 40 ] and G. juniper-virginianae [ 33 ] are able to produce CKs, while the molecular mechanisms of rust-derived CKs as well as their roles in rust-plant interactions remain unclear.…”