Symbiont-mediated adaptation by planthoppers and leafhoppers to resistant rice varieties

Ferrater, Jedeliza B.; Jong, Peter W. de; Dicke, Marcel; Chen, Yolanda H.; Horgan, Finbarr G.

doi:10.1007/s11829-013-9277-9

Cited by 40 publications

(56 citation statements)

References 77 publications

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“…Under the event of the restricted nitrogen content, these symbionts recycle the excretory material uric acid of the plant-hopper into reusable nitrogenous products. Additionally, they enhance the reproductive investment by the adults and shorten the developmental time of the various stages of the progenies (Ferrater et al, 2013). Finally, many bark beetles also host yeasts inside them, which are implicated in vitamin assimilation in these insects, although the exact mechanism of this is yet to be unraveled (Suh et al, 2008;Houseknecht et al, 2011).…”

Section: Nutrient Provisioning By Yeastsmentioning

confidence: 99%

The microbiome of pest insects: it is not just bacteria

Gurung

Wertheim

Salles

2019

Entomologia Exp Applicata

155

113

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Insects are associated with multiple microbes that have been reported to influence various aspects of their biology. Most studies in insects, including pest species, focus on the bacterial communities of the microbiome even though the microbiome consists of members of many more kingdoms, which can also have large influence on the life history of insects. In this review, we present some key examples of how the different members of the microbiome, such as bacteria, fungi, viruses, archaea, and protozoa, affect the fitness and behavior of pest insects. Moreover, we argue that interactions within and among microbial groups are abundant and of great importance, necessitating the use of a community approach to study microbial–host interactions. We propose that the restricted focus on bacteria very likely hampers our understanding of the functioning and impact of the microbiome on the biology of pest insects. We close our review by highlighting a few open questions that can provide an in‐depth understanding of how other components of the microbiome, in addition to bacteria, might influence host performance, thus contributing to pest insect ecology.

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Section: Nutrient Provisioning By Yeastsmentioning

confidence: 99%

The microbiome of pest insects: it is not just bacteria

Gurung

Wertheim

Salles

2019

Entomologia Exp Applicata

155

113

View full text Add to dashboard Cite

show abstract

“…Many of these defenses are located in the phloem, including secondary chemicals and herbivore-induced defense hormones such as jasmonic (JA) and salicylic acids (SA) or enzyme-blocking molecules such as proteinase inhibitors (Behmer et al, 2013;Du et al, 2015;Fujita, Kohli, & Horgan, 2013). It is now apparent that phloem-feeding insects depend on a range of facultative or obligate symbiotic microorganisms, including bacteria and fungi, to overcome the nutritional deficiencies and defenses of phloem (Douglas, 1998;2009;Ferrater, Jong, Dicke, Chen, & Horgan, 2013;Hansen & Moran, 2014;Noda et al, 2012;Sasaki, Kawamura, & Ishikawa, 1996;Wan et al, 2014). Furthermore, a number of studies suggest that endosymbiotic bacteria and yeasts might determine host preferences among phloem feeders (Ferrari, Scarborough, & Godfray, 2007;Ferrari, West, Via, & Godfray, 2012;Ferrater et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

“…However, the widespread and rapid adaptation by target herbivores to resistant hosts is a major challenge for crop breeders and seriously limits the effectiveness and durability of resistant crop varieties (e.g., aphids on wheat, planthoppers, and leafhoppers on rice [Haley, Peairs, Walker, Rudolph, & Randolph, 2004;Hirae, Fukuta, Tamura, & Oya, 2007;Horgan, 2018;Horgan et al, 2015Horgan et al, , 2018Vu et al, 2014]). Recent studies that examined the microbiomes of insect herbivores, particularly the rice planthopper, Nilaparvata lugens, reared-on or adapted to contrasting host plant genotypes have suggested that microbiomes change (structurally or functionally) during selection and possibly determine adaptation (Ferrater et al, 2013(Ferrater et al, , 2015Ojha, Sinha, Padmakumari, Bentur, & Nair, 2017;Wang et al, 2015). However, Ferrater et al (2013) indicated that to date, most studies that seek associations between endosymbionts and herbivore virulence have only described microbiomes from two or three insect colonies or samples, each reared on a different host plant (e.g., Chen et al, 2011;Lu et al, 2004;Ojha et al, 2017;Tang et al, 2010;Xu et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

“…Recent studies that examined the microbiomes of insect herbivores, particularly the rice planthopper, Nilaparvata lugens, reared-on or adapted to contrasting host plant genotypes have suggested that microbiomes change (structurally or functionally) during selection and possibly determine adaptation (Ferrater et al, 2013(Ferrater et al, , 2015Ojha, Sinha, Padmakumari, Bentur, & Nair, 2017;Wang et al, 2015). However, Ferrater et al (2013) indicated that to date, most studies that seek associations between endosymbionts and herbivore virulence have only described microbiomes from two or three insect colonies or samples, each reared on a different host plant (e.g., Chen et al, 2011;Lu et al, 2004;Ojha et al, 2017;Tang et al, 2010;Xu et al, 2015). This design confounds microbiome variability between different herbivore populations and microbiome responses to host feeding.…”

Section: Introductionmentioning

confidence: 99%

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Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines

Horgan

Srinivasan

Crisol‐Martínez

et al. 2019

Ecology and Evolution

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The microbiomes of phloem‐feeding insects include functional bacteria and yeasts essential for herbivore survival and development. Changes in microbiome composition are implicated in virulence adaptation by herbivores to host plant species or host populations (including crop varieties). We examined patterns in adaptation by the green leafhopper, Nephotettix virescens, to near‐isogenic rice lines (NILs) with one or two resistance genes and the recurrent parent T65, without resistance genes. Only the line with two resistance genes was effective in reducing leafhopper fitness. After 20 generations on the resistant line, selected leafhoppers attained similar survival, weight gain, and egg laying to leafhoppers that were continually reared on the susceptible recurrent parent, indicating that they had adapted to the resistant host. By sequencing the 16s rRNA gene, we described the microbiome of leafhoppers from colonies associated with five collection sites, and continually reared or switched between NILs. The microbiomes included 69–119 OTUs of which 44 occurred in ≥90% of samples. Of these, 14 OTUs were assigned to the obligate symbiont Candidatus sulcia clade. After 20 generations of selection, collection site had a greater effect than host plant on microbiome composition. Six bacteria genera, including C. sulcia, were associated with leafhopper virulence. However, there was significant within‐treatment, site‐related variability in the prevalence of these taxa such that the mechanisms underlying their association with virulence remain to be determined. Our results imply that these taxa are associated with leafhopper nutrition. Ours is the first study to describe microbiome diversity and composition in rice leafhoppers. We discuss our results in light of the multiple functions of herbivore microbiomes during virulence adaptation in insect herbivores.

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“…The brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), causes hopper burn damage on rice plants and transmits rice viruses, causing enormous yield loss . The use of chemical insecticides and resistant rice varieties has been adequate for controlling BPH, but there is a wide‐scale resurgence of the pest, as N. lugens has developed medium‐to‐high resistance to these control measures in recent years . For example, the overuse of pesticides such as buprofezin and imidacloprid has led to a loss of BPH control in China over the last decade .…”

Section: Introductionmentioning

confidence: 99%