Molecular profiling of the Mahanarva spectabilis salivary glands and phytohormonal response of elephant grass

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ORIGINAL RESEARCH ARTICLE

Molecular profiling of the Mahanarva spectabilis salivary glands and phytohormonal response of elephant grass Nayara B. Saraiva 1 & Nayara B. Emidio 2 & Camilo E. Vital 1,3 & Michélia A. N. Gusmão 2 & Danielle G. Marconato 2 & Flaviane Silva Coutinho 1,3 & Jorge Fernando Pereira 4 & Alexander Machado Auad 4 & Priscila Faria-Pinto 2 & Humberto J. O. Ramos 1,3 & Maria Goreti Almeida Oliveira 1 Received: 23 June 2019 / Accepted: 18 September 2020 # African Association of Insect Scientists 2020

Abstract Signal perception in plants is determinant to trigger specific physiological changes that confer resistance during the early stages of the insect attack. Thus, molecular characterization of both insect effectors and plant hormonal regulators are essential in developing forage grasses resistant to infestation by spittlebug Mahanarva spectabilis. We evaluated the presence of effectors in the salivary glands of M. spectabilis that could enable the infestation of elephant grass (Pennisetum purpureum). The presence of an NTPDase-like enzyme was confirmed, and higher activity was observed in females that hydrolyzed ADP. High levels of long chain fatty acids, such as octadecanoid acid (19.5%), prostaglandin A2 (4.7%), eicosanoid acid and the phytohormone salicylic acid (~4.0 μg/g) were also detected in the salivary glands. After 24 h of infestation, the phytohormone profiles were altered in leaves damaged by M. spectabilis, suggesting that the insect effectors modulate the plant response. Our results suggest that the plant response modulation may be the result of crosstalk between the salicylic acid, jasmonic acid, abscisic acid and zeatin pathways, induced by molecules from the salivary glands. This shows that the spittlebugs can interfere with jasmonic acid and zeatin accumulation in elephant grass plants. Keywords Spittlebugs . Plant resistance . Fatty acids . Apyrase . Phytohormone, metabolomics

Introduction Molecules secreted by salivary gland of insects during infestation leads to a significant metabolic reprogramming of the Humberto J. O. Ramos and Maria Goreti Almeida Oliveira contributed equally to this work. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s42690-020-00275-9) contains supplementary material, which is available to authorized users. * Humberto J. O. Ramos [email protected] 1

Department of Biochemistry and Molecular Biology, Laboratory of Enzymology, Biochemistry of Proteins and Peptides, BIOAGRO/ INCT-IPP, Universidade Federal de Viçosa, UFV, Viçosa, Brazil

2

Department of Biochemistry, Laboratory of Protein Structure and Function, Federal University of Juiz de Fora, UFJF, Juiz de Fora, Brazil

3

Center of Analysis of Biomolecules, NuBioMol, Universidade Federal de Viçosa, UFV, Viçosa, Brazil

4

Embrapa Gado de Leite, Juiz de Fora, Brazil

plant metabolism shaping its defense response (Gatehouse 2002; Nguyen et al. 2016). These molecules might include herbivore-associated molecular patterns (HAMPs), which are produced by herbi