Dynamic metabolic responses of brown planthoppers towards susceptible and resistant rice plants

Abstract

SummaryBrown planthopper (Nilaparvata lugens Stål, BPH) causes huge economic losses in rice‐growing regions, and new strategies for combating BPH are required. To understand how BPHs respond towards BPH‐resistant plants, we systematically analysed the metabolic differences between BPHs feeding on the resistant and susceptible plants using NMR and GC‐FID/MS. We also measured the expression of some related genes involving glycolysis and biosyntheses of trehalose, amino acids, chitin and fatty acids using real‐time PCR. BPH metabonome was dominated by more than 60 metabolites including fatty acids, amino acids, carbohydrates, nucleosides/nucleotides and TCA cycle intermediates. After initial 12 h, BPHs feeding on the resistant plants had lower levels of amino acids, glucose, fatty acids and TCA cycle intermediates than on the susceptible ones. The levels of these metabolites recovered after 24 h feeding. This accompanied with increased level in trehalose, choline metabolites and nucleosides/nucleotides compared with BPH feeding on the susceptible plants. Decreased levels of BPH metabolites at the early feeding probably resulted from less BPH uptakes of sap from resistant plants and recovery of BPH metabolites at the later stage probably resulted from their adaptation to the adverse environment with their increased hopping frequency to ingest more sap together with contributions from yeast‐like symbionts in BPHs. Throughout 96 h, BPH feeding on the resistant plants showed significant up‐regulation of chitin synthase catalysing biosynthesis of chitin for insect exoskeleton, peritrophic membrane lining gut and tracheae. These findings provided useful metabolic information for understanding the BPH–rice interactions and perhaps for developing new BPH‐combating strategies.

Combined Metabonomic and Quantitative RT-PCR Analyses Revealed Metabolic Reprogramming Associated with Fusarium graminearum Resistance in Transgenic Arabidopsis thaliana

“…This is conceivable since Phe, Tyr, and Trp are precursors for biosynthesis of phenylpropanoids and tryptophan-related alkanoids which have antibacterial activity in plant resistance to biotic stressors (Abdel-Farid et al, 2009 ). Biosynthesis of osmolytes such as glucose, myo -inositol, betaine, and proline are important metabolic reprogramming strategy for plant resistance to both abiotic and biotic stressors (Choi et al, 2004 ; Browne and Brindle, 2007 ; Paranidharan et al, 2008 ; Bollina et al, 2010 ; Dai et al, 2010b ; Liu et al, 2010 , 2017 ; Zhang et al, 2011 ; Kumar et al, 2016 ).…”

“…Metabonomic analysis of wheat leaves and stem tissues indicated that the levels of betaine, sucrose, glucose, glutamate, glutamine, alanine, trans -aconitic acid and some aromatic compounds were positively correlated with FHB resistance (Browne and Brindle, 2007 ). Metabolomic phenotypes have also been reported for numerous plant-pathogen interactions including Brachypodium distachyon and Magnaporthe grisea (William Allwood et al, 2006 ), mulberry leaf and phytoplasma (Gai et al, 2014 ), BPH infestation of rice (Liu et al, 2010 , 2017 ), FG infected barley (Bollina et al, 2010 ), and wheat (Browne and Brindle, 2007 ; Paranidharan et al, 2008 ) together with chick pea (Kumar et al, 2016 ).…”

“…Previous works have already shown metabonomics as a potentially powerful tool for obtaining the detailed metabolic responses of plants toward both biotic and abiotic stressors (Choi et al, 2004 ; Browne and Brindle, 2007 ; Paranidharan et al, 2008 ; Allen et al, 2009 ; Bollina et al, 2010 ; Dai et al, 2010b ; Liu et al, 2010 , 2017 ; Zhang et al, 2011 ; Sanchez et al, 2012 ; Kumar et al, 2016 ; Glaubitz et al, 2017 ). Tyrene-acrylic esters and indole-related alkaloids were found to be the main metabolites of Catharanthus roseus (L.) differentiating healthy leaves from the ones infected by ten different phytoplasma organisms (Choi et al, 2004 ).…”

NMR metabolite comparison of local pigmented rice in Yogyakarta

“…The TSP was used as a reference at δ 0.00. The metabolites were identified based on the 1 H-NMR spectra and comparisons with the NMR spectra of the reference compounds and published literatures (Fan 1996;Dai et al 2010;Kim et al 2010;Jones et al 2011;Nuringtyas et al 2012;Nam et al 2015;Uawisetwathana et al 2015;Liu et al 2017;Pramai et al 2017).…”

Phenotypic and transcriptomic responses of two Nilaparvata lugens populations to the Mudgo rice containing Bph1

“…Resistant rice varieties have been reported to have significant effects on the overall BPH fitness, including feeding periods, survival, metamorphosis, and fecundity 20,21 . For instance, during the compatible rice-BPH interactions, probing and pathway (N 1 + N 2 + N 3 ) phases have been reported to be much shorter as compared to that of during the incompatible interactions 22 .…”