Modern Maize Hybrids Have Lost Volatile Bottom-Up and Top-Down Control of Dalbulus maidis , a Specialist Herbivore

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Modern Maize Hybrids Have Lost Volatile Bottom-Up and Top-Down Control of Dalbulus maidis, a Specialist Herbivore María Victoria Coll-Aráoz 1,2 & Jorge G. Hill 1 & Erica Luft-Albarracin 1 & Eduardo G. Virla 1,3 & Patricia C. Fernandez 4,5 Received: 29 May 2020 / Revised: 29 May 2020 / Accepted: 20 July 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Following damage by herbivores, many plants release volatiles that dissuade future conspecifics from feeding. In many crop plants however, induced volatiles mediating this kind of interactions among plants, herbivores and also their natural enemies have been altered through the process of domestication. The selection of crops for increased yield may have gone at a cost of defense, possibly including defense-related volatiles. Dalbulus maidis (Hemiptera: Cicadellidae), a specialist leafhopper that only feeds on Zea spp., is a vector of Corn Stunt Spiroplasma, a serious maize disease. Here, we compared the volatiles released following D. maidis attack by a maize landrace and two maize hybrids of temperate and tropical background. Also, we performed behavioral assays with the leafhopper contrasting healthy nonattacked maize seedlings versus attacked seedlings. The maize landrace produced more than 6-fold larger quantities of induced volatiles compared to the maize hybrids after herbivory. Corn leafhopper females were able to detect and significantly preferred the odors of healthy seedlings over the attacked ones only in the landrace. They did not discriminate between the attacked and non-attacked hybrids. Additionally, we found that the attraction of the parasitoid wasp Anagrus virlai (Hymenoptera: Mymaridae) to its host was diminished in the tested hybrids. The parasitoid was able to detect the odors of the attacked landrace, however it was unable to discriminate between healthy and attacked maize hybrid plants. These results suggest that those more domesticated germplasms may have lost the ability not only to release volatiles that avoid colonization of future herbivores, but also to attract their natural enemies in a tritrophic system. Keywords Domestication . Volatile organic compounds . Tritrophic interaction . Anagrus . Corn stunt Spiroplasma . Agronomic selection . Herbivore resistance

Introduction Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10886-020-01204-3) contains supplementary material, which is available to authorized users. * Patricia C. Fernandez [email protected] 1

PROIMI-Biotecnología, Av. Belgrano y Pje. Caseros, S.M. de Tucumán, Tucumán, Argentina

2

Facultad de Ciencias Naturales e IML, UNT, Miguel Lillo, 205 S.M. de Tucumán, Argentina

3

Instituto de Entomología, Fundación M Lillo, Miguel Lillo, 251 S.M. de Tucumán, Argentina

4

Centro de Investigaciones en Hidratos de Carbono, CIHIDECAR-CONICET, Buenos Aires, Argentina

5

Facultad de Agronomía, Universidad de Buenos Aires, Av. San Martin, 4453 Buenos Aires, Argentina

In response to herbivory, many plants