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Frontiers of Agricultural Science and Engineering

ISSN 2095-7505

ISSN 2095-977X(Online)

CN 10-1204/S

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Front. Agr. Sci. Eng.    2021, Vol. 8 Issue (2) : 292-301    https://doi.org/10.15302/J-FASE-2021395
RESEARCH ARTICLE
CHARACTERISTICS OF HERBIVORY/WOUND-ELICITED ELECTRICAL SIGNAL TRANSDUCTION IN TOMATO
Chaoyi HU1, Siqi DUAN1, Jie ZHOU1, Jingquan YU1,2()
1. Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, China.
2. Key Laboratory of Horticultural Plant Growth and Development, Ministry of Agriculture and Rural Affairs of China, Hangzhou 310058, China.
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Abstract

• Herbivory and mechanical wounding elicited electrical signals.

• Petiole wounding elicited stronger electrical signals than did leaflet wounding.

• Leaflet wounding elicited electrical signals and JA signaling within a compound leaf.

• GLR3.3 and GLR3.5 mediated leaflet-to-leaflet electrical signal transduction.

• JA synthesis and Helicoverpa armigera resistance were reduced in glr3.3/3.5 plants.

Electrical signals commonly occur in plants in response to various environmental changes and have a dominant function in plant acclimation. The transduction of wound-elicited electrical signals in the model plant species Arabidopsis has been characterized but the characteristics of electrical signal transduction in response to herbivory or wounding in crop species remain unknown. Here, the features of electrical signals elicited by insect herbivory and wounding in tomato were investigated. Unlike those in Arabidopsis, wounding tomato leaves did not cause leaf-to-leaf electrical signal transduction. In contrast, electrical signals elicited in response to petiole wounding were stronger and more strongly transduced. Leaflet wounding also activated electrical signal transduction and jasmonic acid (JA) signaling within the whole compound leaf. It was also demonstrated that tomato glutamate receptor-like 3.3 (GLR3.3) and GLR3.5 mediated leaflet-to-leaflet electrical signal transduction. Herbivory-induced JA accumulation and Helicoverpa armigera resistance were reduced in glr3.3/3.5 plants. This work reveals the nature of electrical signal transduction in tomato and emphasizes the key roles of GLR3.3 and GLR3.5 in electrical signal transduction and JA signaling activation.
Keywords electrical signal      glutamate receptor-like      herbivory      jasmonic acid      tomato     
Corresponding Author(s): Jingquan YU   
Just Accepted Date: 30 April 2021   Online First Date: 24 May 2021    Issue Date: 13 July 2021
 Cite this article:   
Chaoyi HU,Siqi DUAN,Jie ZHOU, et al. CHARACTERISTICS OF HERBIVORY/WOUND-ELICITED ELECTRICAL SIGNAL TRANSDUCTION IN TOMATO[J]. Front. Agr. Sci. Eng. , 2021, 8(2): 292-301.
 URL:  
https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2021395
https://academic.hep.com.cn/fase/EN/Y2021/V8/I2/292
Fig.1  Insect herbivory induced changes in the surface potential of tomato leaves. (a) Experimental design for measuring electrical signals elicited by herbivory on a leaf. Measuring electrodes: P1, midrib; P2, petiole; P3, petiole of the first leaf. Helicoverpa armigera larvae were allowed to feed at a position about 1 cm from electrode P1. (b) Electrical signals measured at electrodes P1, P2 and P3 of (a). (c) Experimental design for measuring electrical signals elicited by herbivory of the petiole. Measuring electrodes: P1, petiole (1 cm from the larval herbivory site); P2, petiole (1 cm from P2); P3, midpoint of the midrib of the terminal leaflet. (d) Electrical signals measured at electrodes P1, P2 and P3 of (c). The starting time of larval herbivory is indicated with a filled triangle. For (b) and (d), typical surface potential changes are shown (n = 6).
Fig.2  Electrical signals caused by leaf wounding and petiole wounding. (a) Experimental design for measuring electrical signals elicited by mechanical wounding of a leaf. Measuring electrodes: P1, midrib 1 cm from the wounding position; P2, midrib 2 cm from electrode P1; P3, junction of the terminal leaflet and petiole. Dashed line, position of the mechanical wounding of one-third of the terminal leaflet. (b) Electrical signals measured at electrodes P1, P2 and P3 of (a). (c) Experimental design for measuring electrical signals activated by mechanical wounding of the petiole. Measuring electrodes: P1 (petiole 1 cm from the wound position; P2, the junction of the terminal leaflet and petiole; P3, the midpoint of the midrib of the terminal leaflet. Dashed line, position of the mechanical wound of the petiole. (d) Electrical signals measured at electrodes P1, P2 and P3 of (c). For (b) and (d), typical surface potential changes are shown (n = 12).
Position P1 P2 P3 Speed (cm·min−1)
Amplitude (mV) x/n Amplitude (mV) x/n Amplitude (mV) x/n
Leaf wound −26.32±10.76 a 9/12 −14.78±7.48 a 5/12 −14.74±2.53 a 3/12 6.91±2.52
Petiole wound −39.33±9.31 a 12/12 −16.43±13.10 b 8/12 −14.17±5.22 b 3/12 10.05±4.14
Tab.1  Amplitude and speed of leaf and petiole wound-elicited electrical signals
Fig.3  GLR mutants present reduced amplitude and transduction of electrical signals. (a) Experimental design for measuring electrical signals within a compound leaf. Measuring electrodes: P1, junction of the petiole and leaflet 1; P2, junction of the petiole and leaflet 2; P3, junction of the petiole and leaflet 3. Dashed line, position of the mechanical wound at the center of leaflet 1. L1, leaflet 1; L2, leaflet 2; L3, leaflet 3. (b) Electrical signals measured at P1, P2 and P3 in untransformed plants. (c) Electrical signals measured at P1, P2 and P3 in glr3.3 mutants. (d) Electrical signals measured at P1, P2 and P3 in glr3.5 mutants. (e) Electrical signals measured at P1, P2 and P3 in glr3.3/3.5 double mutants. For (b–e), typical surface potential changes are shown (n = 10).
Position P1 P2 P3
Amplitude (mV) x/n Amplitude (mV) x/n Amplitude (mV) x/n
WT −43.21±15.25 a 10/10 −36.94±18.67 5/10 −6.12±1.89 4/10
glr3.3 −38.37±18.13 a 10/10 −20.78±14.60 2/10 / 0/10
glr3.5 −17.10±3.64 b 10/10 / 0/10 / 0/10
glr3.3/3.5 −13.11±6.71 b 10/10 −8.26±2.08 2/10 / 0/10
Tab.2  Amplitude of electrical signals in GLR mutants
Fig.4  L1 Wounding induced JA biosynthesis and signaling-related gene expression within compound leaves. (a) Transcript level of LOXD after L1 wounding. (b) Transcript level of AOC after L1 wounding. (c) Transcript level of OPR3 after L1 wounding. (d) Transcript level of JAZ10 after L1 wounding. Samples were collected 45 min after L1 wounding. Three biological samples were used for qRT-PCR determination. ACTIN2 and UBI3 were used as internal references to calculate the relative expression of the target genes, and the gene expression in L1/L2/L3 under control conditions was defined as 1. The data represent the mean±SD (n = 3). L1, leaflet 1; L2, leaflet 2; L3, leaflet 3. Statistically significant differences are indicated with asterisks (*, P<0.05; **, P<0.01) according to Student’s t-test.
Fig.5  GLR mutants present reduced herbivory-induced JA and JA-Ile accumulation and Helicoverpa armigera resistance. (a) JA and JA-Ile contents in WT plants and glr3.3/3.5 mutants upon W+ OS. Samples were collected 1 h after W+ OS. Three biological samples were used. The data represent the mean±SD (n = 3). The means denoted by the same letter do not significantly differ at P<0.05 according to Tukey’s test. (b) Mean weight increase (upper panel) and representative images of larvae after 3 d of herbivory on glr3.3 and glr3.5 single mutants and on glr3.3/3.5 double mutants (lower panel). The data represent the mean±SD (n = 24). Bar= 1 cm.
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