Plant-derived CO₂mediates long-distance host location and quality assessment by a root herbivore

Abstract

Insect herbivores can use volatile and visual cues to locate and select suitable host plants from a distance. The importance of CO 2 , arguable the most conserved volatile marker of metabolic activity, is not well understood in this context, even though many herbivores are known to respond to minute differences in CO 2 concentrations. To address this gap of knowledge, we manipulated CO2 perception of the larvae of the western corn rootworm (Diabrotica virgifera virgifera; WCR) through RNA interference and studied how CO 2 perception impacts their interaction with their host plant, maize (Zea mays). We show that the expression of a putative Group 2 carbon dioxide receptor, DvvGr2, is specifically required for larval responses to CO2. Silencing DvvGr2 has no major effect on the ability of WCR larvae to locate host plants at short distance (<10 cm), but increasingly impairs host location at greater distances, suggesting that WCR larvae integrate CO 2 with other volatile cues for host finding in a distance-specific manner. We further show that the larvae use CO 2 as a fitnessrelevant long-distance indicator of plant nutritional status: Maize plants that are well-fertilized emit more CO2 from their roots and are better hosts for WCR than plants that are nutrient-deficient, and the capacity of WCR larvae to distinguish between these plants depends exclusively on their capacity to perceive CO 2 through DvvGr2. This study unravels how CO 2 can mediate plant-herbivore interactions by serving as a distance-dependent host location and quality assessment cue.Keywords: Plant-herbivore interactions, foraging, volatile perception, behaviour, host location. 2012).So far, this model has not been experimentally validated, and the precise role of plant-derived CO2 as a host location cue by herbivores in general, and root herbivores in particular, remains unclear (Eilers et al., 2016). To the best of our knowledge, no studies so far have investigated the role of plant-derived CO 2 in plant-herbivore interactions in vivo using molecular manipulative approaches.The larvae of Diabrotica virgifera virgifera (western corn rootworm, WCR) feed exclusively on maize roots and cause major yield losses in the US and Eastern Europe (Ciosi et al., 2008; Gray et al., 2009; Meinke et al., 2009; Toepfer et al., 2015). The larvae rely on a number of volatile and non-volatile chemicals to identify and locate host plants, distinguish between suitable and less-suitable maize plants and forage within the maize root system (Hiltpold et al., 2013; Johnson and Gregory, 2006; Johnson and Nielsen, 2012; Robert et al., 2012c; Schumann et al., 2018). Non-volatile primary metabolites such as sugars and fatty acids as well as secondary metabolites such as benzoxazinoids and phenolic acid conjugates modulate larval behaviour (Bernklau et al., 2011; Bernklau et al., 2015; Bernklau et al., 2016a; Bernklau et al., 2018b; Erb et al., 2015a; Hu et al., 2018; Huang et al., 2017; Robert et al., 2012c). Volatiles including (E)-βcaryophyllene, ethylene and CO2 attra...

Candidate Chemosensory Genes Identified in the Adult Antennae of Sympiezomias velatus and Binding Property of Odorant-Binding Protein 15

“…Whether this finding means that the SvelGR3-encoding gene was truly lost and S. velatus thus lost the related ability remains unclear. A recent study on the larvae of a chrysomelid root herbivore, Diabrotica virgifera , showed that GR2 is responsible for the perception of plant-derived CO 2 and plays a crucial role in long-distance host location and assessment of the plant nutritional status ( Arce et al, 2020 ). Whether S. velatus GRs have similar physiological or behavioral functions is worth further study.…”

Western Corn Rootworm, Plant and Microbe Interactions: A Review and Prospects for New Management Tools

“…It may also be possible to utilize knowledge of the factors influencing host plant establishment for management in the future. WCR larvae orient towards maize roots following CO 2 gradients and can detect concentrations as low as 2 mmol/mol [ 27 , 28 , 29 ]. In choice tests, significantly more neonate WCR larvae were attracted to synthetic CO 2 with a concentration of 11.2 mmol/mol than to growing maize with a CO 2 concentration of 1.36 mmol/mol [ 29 ].…”

Complex plant metabolomes guide fitness-relevant foraging decisions of a specialist herbivore

“…3D). To assess silencing specificity, we measured the transcription of the putative CO2-receptor DvvGr2 (67). Feeding dsRNA targeting DvvGr43a did not change the transcript abundance of DvvGr2 (Fig.…”

“…Western corn rootworm larvae respond behaviorally to a wide variety of chemical cues, including CO2 (60), sugars and fatty acids (61,62), aromatic and terpene volatile organic compounds (63,64), conjugated phenolic acids (65) and benzoxazinoids (66). The emerging picture is that these chemicals likely allow western corn rootworm larvae to locate plant roots from a distance (67), to discriminate between plants of different quality (63)(64)(65)68), and to identify and feed on the most nutritious roots (66,69). Several in vitro experiments also suggest that the western corn rootworm can integrate multiple chemical cues for host finding and acceptance (61), hinting at the substantial sensory capacity of this specialist root feeder.…”