Whitefly infestation of pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the below‐ground microflora

Abstract

Summary1. Upon facing biotic stresses, plants orchestrate defence mechanisms via internal and external mechanisms that are mediated by signalling molecules such as salicylic acid, jasmonic acid, ethylene and various other volatile compounds. Although pathogen-and chemical-induced plant resistance has been studied extensively within the same plant compartment, the effects of above-ground (AG) insect-elicited plant defence on the resistance expression in roots and the below-ground (BG) microbial community are not well understood. 2. We assessed the effect of AG whitefly (Bemisia tabaci) attack on the elicitation of induced resistance against a leaf pathogen, Xanthomonas axonopodis pv. vesicatoria, a soil-borne pathogen, Ralstonia solanacearum, and on BG modifications of the rhizosphere microflora in peppers (Capsicum annuum). 3. Symptom development caused by the two bacterial pathogens on leaves and roots was significantly reduced in whitefly-exposed plants as compared to controls. A combined treatment with benzothiadiazole (BTH) and whitefly caused an additive effect on induced resistance, indicating that whitefly-induced plant defence can utilize salicylic acid (SA)-dependent signalling. To obtain further genetic evidence of this phenomenon, we evaluated the gene expression of Capsicum annuum pathogenesis-related protein (CaPR) 1, CaPR4, CaPR10 and Ca protease inhibitor II, and observed increased expression after BTH and ⁄ or whitefly treatment indicating that AG whitefly infestation elicited SA and jasmonic acid signalling in AG and BG. Since the expression pattern of PR genes in the roots differed, we assessed microbial diversity in plants treated with BTH and ⁄ or whitefly. 4. In addition to eliciting BG defence responses, a whitefly infestation of the leaves augmented the population of root-associated Gram-positive bacteria and fungi, which may have positively affected plant growth and induced systemic resistance. Whitefly feeding reduced plant size, which usually occurs as a consequence of the high costs of direct resistance induction. 5. Synthesis. Our results demonstrate that whitefly-induced resistance against bacterial pathogens can cross the AG-BG border and may cause further indirect benefits on future plant development, because it can positively affect the association or plant roots with putatively beneficial microorganisms.Key-words: above-ground, below-ground, plant growth-promoting rhizobacteria, plant-herbivore interactions, Ralstonia solanacearum, whitefly, Xanthomonas axonopodis *Correspondence author. E-mail: cmryu@kribb.re.kr † These authors contributed equally to this study.

Insect stings to change gear for healthy plant: Improving maize drought tolerance by whitefly infestation

“…15 Previous reports revealed that whitefly mainly manipulates the SA-mediated plant defense machinery in Arabidopsis, pepper, and tobacco. 13,14,17 By contrast, JA is the main regulator in maize plants whose accumulation is triggered by aboveground whitefly infestation. 15 This discrepancy may have several explanations.…”

“…infestation activates defense responses against two bacterial pathogens in leaf and root. 13 Recently, whitefly-infested Nicotiana benthamiana plants have shown to produce SA as a way to attenuate Agrobacterium infection. 14 Whitefly infestation positively modulates tobacco defense responses, and infested plants show reduced crown gall formation by Agrobacterium.…”

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

“…Upon insect infestation, plants release compounds such as hormones, exogenous volatile organic compounds, and secondary metabolites as long-distance root-to-shoot signals (for review, see Erb et al, 2009). Whitefly infestation of pepper (Capsicum annuum) plants elicits SAdependent signaling in leaves whereas roots showed increased colonization of Gram-positive bacterial populations (Yang et al, 2011), suggesting a signaling event between aboveground and belowground plant parts. Whereas considerable data exist on the occurrence of aboveground/belowground communication in the case of plant herbivory, evidence of similar phenomena in plant-pathogenic bacteria interactions is lacking.…”

Modulation of Quorum Sensing in Acyl-homoserine Lactone-Producing or -Degrading Tobacco Plants Leads to Alteration of Induced Systemic Resistance Elicited by the Rhizobacterium Serratia marcescens 90-166

“…The root colonization capacity of each root was determined by plating a dilution series onto 1/10 strength TSA and incubating plates for 2−3 days at 30 o C. The population density of Gram-negative bacteria was determined by counting colonies on 1/10 TSA plates supplemented with 10 mg/mL vancomycin to inhibit growth of Gram-positive bacteria. The population density of Gram-positive bacteria was determined by counting colonies on plates that were heat treated at 80 o C for 30 min to kill Gram-negative bacteria and fungal spores (Yang et al, 2011).…”