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Review
. 2009 Feb;103(4):655-63.
doi: 10.1093/aob/mcn127. Epub 2008 Jul 26.

Indirect suppression of photosynthesis on individual leaves by arthropod herbivory

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Review

Indirect suppression of photosynthesis on individual leaves by arthropod herbivory

Paul D Nabity et al. Ann Bot. 2009 Feb.

Abstract

Background: Herbivory reduces leaf area, disrupts the function of leaves, and ultimately alters yield and productivity. Herbivore damage to foliage typically is assessed in the field by measuring the amount of leaf tissue removed and disrupted. This approach assumes the remaining tissues are unaltered, and plant photosynthesis and water balance function normally. However, recent application of thermal and fluorescent imaging technologies revealed that alterations to photosynthesis and transpiration propagate into remaining undamaged leaf tissue.

Scope and conclusions: This review briefly examines the indirect effects of herbivory on photosynthesis, measured by gas exchange or chlorophyll fluorescence, and identifies four mechanisms contributing to the indirect suppression of photosynthesis in remaining leaf tissues: severed vasculature, altered sink demand, defence-induced autotoxicity, and defence-induced down-regulation of photosynthesis. We review the chlorophyll fluorescence and thermal imaging techniques used to gather layers of spatial data and discuss methods for compiling these layers to achieve greater insight into mechanisms contributing to the indirect suppression of photosynthesis. We also elaborate on a few herbivore-induced gene-regulating mechanisms which modulate photosynthesis and discuss the difficult nature of measuring spatial heterogeneity when combining fluorescence imaging and gas exchange technology. Although few studies have characterized herbivore-induced indirect effects on photosynthesis at the leaf level, an emerging literature suggests that the loss of photosynthetic capacity following herbivory may be greater than direct loss of photosynthetic tissues. Depending on the damage guild, ignoring the indirect suppression of photosynthesis by arthropods and other organisms may lead to an underestimate of their physiological and ecological impacts.

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Figures

F<sc>ig</sc>. 1.
Fig. 1.
Conceptual model of the direct effect of herbivory (removal of leaf area) and the indirect effects of herbivore damage to foliage on photosynthesis in the remaining leaf tissues.
F<sc>ig</sc>. 2.
Fig. 2.
False colour images of the location of damage classes surrounding holes in an arabidopsis leaf exposed to herbivory by Trichoplusia ni larvae. Transgenic Arabidopsis thaliana carried a cinnamate-4-hydroxylase (C4H) promoter and β-glucuronidase (GUS) reporter gene fusion. In A. thaliana, enzymes in the phenylpropanoid pathway may contribute to defence against pathogens; C4H is constitutively expressed in the veins of undamaged leaves and induced by wounding near the site of damage. The image was constructed by combining independent images of the same leaf of chlorophyll fluorescence (ΦPSII) and GUS staining for C4H activity using geographic image analysis software. The false-colour scale bars indicate the mean value of ΦPSII for each damage class. The veins shown in blue and purple were classes that were excluded from analysis because their high level of GUS staining was not related to herbivory. Data were generously provided by Dr Jennie Tang.

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