Opposing Roles of Foliar and Glandular Trichome Volatile Components in Cultivated Nightshade Interaction with a Specialist Herbivore

Abstract

Plant chemistry is an important contributor to the interaction with herbivores. Here, we report on a previously unknown role for foliar and glandular trichome volatiles in their interaction with the specialist herbivore of solanaceous plants, the tomato red spider mite Tetranychus evansi. We used various bioassays and chemical analyses including coupled gas chromatography-mass spectrometry (GC/MS) and liquid chromatography coupled to quadrupole time of flight mass spectrometry (LC-QToF-MS) to investigate this interaction between cultivated African nightshades and T. evansi. We show that, whereas morphologically different cultivated African nightshade species released similar foliar volatile organic compounds (VOCs) that attracted T. evansi, VOCs released from exudates of ruptured glandular trichomes of one nightshade species influenced local defense on the leaf surface. VOCs from ruptured glandular trichomes comprising mainly saturated and unsaturated fatty acids deterred T. evansi oviposition. Of the fatty acids, the unsaturated fatty acids accounted for >40% of the oviposition deterrent activity. Our findings point to a defense strategy in a plant, based on opposing roles for volatiles released by foliar and glandular trichomes in response to attack by a specialist herbivore.

Fig 1. Olfactory responses of Tetranychus evansi females to intact plant volatile odors of three African nightshade species.

(a) Intact plants compared to air (control); and b) Pairwise comparisons of intact plants. Responses are expressed as preference indices (PI); * = significant; ns = not significant (α = 0.05).

Fig 2. Representative chromatograms of chemical components identified in foliar volatiles of three African nightshade species viz. Solanum sarrachoides, S. scabrum and S. villosum.

Peak no: 1 = hexanal; 2 = (Z)-3-hexen-1-ol; 3 = (+)-α-Pinene; 4 = benzaldehyde; 5 = (-)-β-Pinene; 6 = 6-methyl-5-hepten-2-one; 7 = β-myrcene; 8 = octanal; 9 = (S)-(-)-limonene; 10 = undecane; 11 = dihydromyrcenol; 12 = methyl benzoate; 13 = linalool; 14 = nonanal; 15 = isophorone; 16 = octanoic acid; 17 = α-terpineol; 18 = dodecane; 19 = decanal; 20 = carvacrol, methyl ether; 21 = pentadecane; 22 = bornyl acetate; 23 = hexadecane; 24 = copaene; 25 = β-elemene; 26 = longifolene; 27 = (−)-α-cedrene; 28 = (E)-β -caryophyllene; 29 = (+)-β-cedrene; 30 = geranyl acetone; 31 = α-humulene; 32 = butylated hydroxytoluene; 33 = δ-cadinene; 34 = caryophyllene oxide; 35 = cedrol; 36 = hexadecanoic acid.

Fig 3. Abundance and behavioral responses of Tetranychus evansi to chemical components detected in intact plants of the three African nightshade species.

(a) Abundance of compound classes detected from foliar scents of Solanum sarrachoides, S. scabrum and S. villosum; (b) olfactory response of Tetranychus evansi to individual compound classes and a blend of all the classes. All responses were compared to a control and expressed as preference indices; * = significant (α = 0.05).

Fig 4. Bioactivity of glandular trichome exudates obtained from Solanum sarrachoides and tested on Tetranychus evansi females.

(a) Oviposition deterrent activity of glandular trichome components of Solanum sarrachoides to T. evansi. Untreated leaf disks of S. scabrum were used as control in bars I, II and III. Filter paper arenas treated with dichloromethane and methanol were used as control in bars IV and V. Representative chromatograms of chemical components present in glandular trichome exudates dissolved in dichloromethane from: (b) Solanum sarrachoides. Peak no: 1 = 2-undecanone; 2 = decanoic acid; 3 = undecanoic acid; 4 = dodecanoic acid; 5 = myristoleic acid; 6 = tetradecanoic acid; 7 = pentadecanoic acid; 8 = palmitoleic acid; 9 = hexadecanoic acid; 10 = heptadecanoic acid; 11 = linoleic acid; 12 = oleic acid; 13 = octadecanoic acid and (c) S. villosum; and (d) representative chromatogram of chemical components present in glandular trichome exudates of S. sarrachoides dissolved in methanol; Compound no. 1 = quercetin; 2 = 6-hydroxyluteolin; 3 = hesperetin.

Fig 5. Effect of chemical components detected in trichome exudates of S. sarrachoides on oviposition deterrence activity of Tetranychus evansi.

(a) Oviposition deterrence index (ODI) on filter paper arenas treated with blends of 2-undecanone (2-UND), saturated fatty acids (SFA) and unsaturated fatty acids (UNSFA) detected in glandular trichome exudates of S. sarrachoides. (b) Oviposition deterrence index on filter paper arenas treated with a full blend constituting; (I) 2-undecanone, saturated and unsaturated fatty acids at 1000 ng μL^-1 and; (II) a varied concentration of the unsaturated fatty acids at 10 ng μL^-1 whereby 2-undecanone and saturated fatty acids were maintained at 1000 ng μL^-1.