Abstract
Under natural conditions, plants have to cope with numerous stresses, including light-stress and herbivory. This raises intriguing questions regarding possible trade-offs between stress defences and growth. As part of a program designed to address these questions we have compared herbivory defences and damage in wild type Arabidopsis thaliana and two “photoprotection genotypes”, npq4 and oePsbS, which respectively lack and overexpress PsbS (a protein that plays a key role in qE-type non-photochemical quenching). In dual-choice feeding experiments both a specialist (Plutella xylostella) and a generalist (Spodoptera littoralis) insect herbivore preferred plants that expressed PsbS most strongly. In contrast, although both herbivores survived equally well on each of the genotypes, for oviposition female P. xylostella adults preferred plants that expressed PsbS least strongly. However, there were no significant differences between the genotypes in levels of the 10 most prominent glucosinolates; key substances in the Arabidopsis anti-herbivore chemical defence arsenal. After transfer from a growth chamber to the field we detected significant differences in the genotypes’ metabolomic profiles at all tested time points, using GC-MS, but no consistent “metabolic signature” for the lack of PsbS. These findings suggest that the observed differences in herbivore preferences were due to differences in the primary metabolism of the plants rather than their contents of typical “defence compounds”. A potentially significant factor is that superoxide accumulated most rapidly and to the highest levels under high light conditions in npq4 mutants. This could trigger changes in planta that are sensed by herbivores either directly or indirectly, following its dismutation to H2O2.
Highlights
Plants are sedentary organisms and cannot escape unfavourable conditions, they have to cope with a host of biotic and abiotic stresses, such as drought, cold, light, herbivores and pathogens
In all but one comparison, larger leaf areas were consumed of plants with higher PsbS levels, the difference was only significant in the npq4 versus overexpressing PsbS (oePsbS) trial with S. littoralis larvae according to a paired t-tests (p = 0.003)
Interactions between plants and herbivores are enormously complex. They are strongly influenced by numerous environmental variables and there are strong within- and between-species variations, partly due to intricate co-evolution [24,25]
Summary
Plants are sedentary organisms and cannot escape unfavourable conditions, they have to cope with a host of biotic and abiotic stresses, such as drought, cold, light, herbivores and pathogens. Our previous findings indicate that npq plants lacking PsbS under natural conditions may be in a ‘permanently’ induced defence or ‘‘pre-sensitized’’ state that allows them to respond more rapidly to stress [10], which may explain their relatively low seed set in the field [5]. This may be due to the accumulation of one or several ROS species, for example singlet oxygen, superoxide or hydrogen peroxide, which may act as (a) signalling compound(s) and interact with components of other ‘‘stress pathways’’, such as the octadecanoid pathway leading to JA/jasmonate and its derivative methyl jasmonate (MeJa). To explore metabolic differences that may be linked to variations in both PsbS levels and herbivore responses we analysed the genotypes’ global metabolic profiles, as well as their levels and production kinetics of glucosinolates, superoxide and peroxide
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