Performances of survival, feeding behavior and gene expression in aphids reveal their different fitness to host alteration

Abstract

Insect populations feeding on different plant species are under selection pressure to adapt to these differences. A study integrating elements of the ecology, behavior, and gene expression of aphids on different host plants has not yet been well-explored. The present study explores the relationship between host fitness and survival, feeding behavior, and salivary gland gene expression of a pea (Pisum sativum) host race of Acyrthosiphon pisum feeding on a common host Vicia faba and on three genetically-related hosts (Vicia villosa, Medicago truncatula, and Medicago sativa). Life table data indicated that aphids on non-favored hosts exhibited small size, low reproduction rate, slow population increase and individual development, and long lifespan. Electrical penetration graph results showed that the aphids spent significantly less time in passive ingestion of phloem sap on all non-preferred host plants before acclimation. After a period of acclimation on M. truncatula and V. villosa, pea host race individuals showed improved feeding behavior. No individuals of the pea host race completed its life history on M. sativa. Interestingly, the number of host-specific differentially-expressed salivary gland genes was negatively correlated with the fitness of aphids on this host plant. This study provided important cues in host plant specialization in aphids.

An aphid effector promotes barley susceptibility through suppression of defence gene expression

“…It is possible that, unlike the case for plant pathogens 299 where effector gene expression varies across different infections stages (O'Connell et al, 300 2012; Jupe et al, 2013; Hacquard et al, 2013; Cotton et al, 2014), aphid effectors are 301 constitutively expressed to ensure aphids are generally ready to infest a plant. This 302 hypothesis is in line with other reports where no significant overall effector gene 303 expression variation was reported when aphids were adapted to different plant 304 environments(Lu et al, 2016;Mathers et al, 2017;Thorpe et al, 2018). The Rp1/Mp1 305 and Rp58/Mp58 pair was more similarly expressed in the two aphid species relative to the 306 RpC002/MpC002 effector pair.…”

Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species

“…M. persicae clone O successfully colonised all three host species with no significant differences observed in survival and reproduction rates, weight, development time and longevity (Additional file 18 : Figure S9A). This is in contrast to an A. pisum biotype collected from the legume Pisum sativum that had significantly reduced reproduction rates and increased developmental time and overall lower fitness on two other legume species ( Medicago truncatula , Vicia villosa ) compared to the ‘universal’ host ( Vicia faba ), which can be colonised by many pea biotypes [ 40 ]. We analysed the differential expression of M. persicae clone O cathepsin B and RR-2 cuticular protein genes by quantitative real-time polymerase chain reaction (qRT-PCR) to assess if the upregulation and downregulation of these genes upon a host switch can be confirmed by a method other than RNA-seq and to develop an assay that can be used for analyses of differential gene expression in single aphids (see next step).…”

“…Survival rates of the nymphs upon transfer to a different plant species was over 60% and the reproduction rates of these surviving aphids were similar to the aphids that did not experience a host change (Additional file 18 : Figure S9B). In contrast, the A. pisum P. sativum biotype had a remarkable reduction in reproduction rates upon host change to the three legume plants M. truncatula , Vicia villosa and M. sativa and this aphid did not establish stable colonies on the latter legume [ 40 ]. Cathepsin B gene expression went up in M. persicae transferred from N. benthamiana to A. thaliana and down in aphids transferred from A. thaliana to N. benthamiana (Fig.…”

“…Furthermore, we show that disrupting the transcriptional adjustment of a gene family with high levels of differential expression upon host transfer (cathepsin B), using plant-mediated RNAi, has host-dependent fitness costs for M. persicae , suggesting that host-associated transcriptional plasticity is adaptive in M. persicae . Differential gene expression upon host transfer has also been observed in the legume specialist A. pisum [ 40 , 43 ]. However, host switching in A. pisum is restricted to Fabaceae and successful transitions are only possible between a common host ( Vicia faba ) shared among all A. pisum biotypes and a second host, specific to each genetic lineage.…”

Genome of Russian wheat aphid an economically important cereal aphid

“…5 ). The large grouping of genes associated with protein modification and turnover is interesting in that it has been shown previously that phloem feeding aphids, despite low levels of heterogeneity, display various levels of virulence towards single host cultivars [ 40 – 43 ], as is the case for Diuraphis noxia biotypes SA1 and SAM [ 11 , 44 ]. The basis for this observed variance may include the adaptability of the aphid’s salivary cohort in response to its feeding environment [ 45 , 46 ] as this is central to the molecular interaction between aphids and their hosts.…”