Consequences of intra-specific metabolic diversity in plants for soil organisms : a baseline approach for evaluating ecological effects of genetic modifications

P. Kabouw

Research output: Thesisinternal PhD, WU

Abstract

Plant intra-specific variation, i.e. variation within a plant species, is known to affect organisms that are directly associated to plants. These effects may be due to for example differences in nutritional quality or defensive metabolites. Plant intra-specific variation can also affect higher trophic level and organisms not directly associated to the plants, i.e. non-target organisms. These effects occur via differences in the quality of herbivores serving as host or prey, due to differences in the rates of attractiveness for higher trophic level organisms, differences in decomposition rates of litter, or differences in root exudates. Intra-specific variation occurs naturally in wild plant populations and humans have used this to select plants for agricultural use. Breeding and artificial selection for plant traits that were desirable for agricultural practices resulted in novel varieties, adding to intra-specific variation in these species.
In addition to natural variation and variation between cultivars, plant genetic modification can result in crop varieties with novel traits such as increased productivity or insect resistance. These traits may also affect non-target organisms. The question is whether these effects fall within or outside the range of non-target effects observed for conventionally bred varieties. To answer this question, one first needs to determine the range of non-target effects caused by conventional varieties, a so-called ‘baseline’.In this thesis, I examined the baseline effects that conventional white cabbage varieties have on soil organisms, the mechanisms behind these effects, and the consequences for interactions between below-and aboveground organisms. The range of effects observed in the conventionally bred varieties can then serve as a baseline for evaluating the effects of genetic modifications.          
I started by examining intra-specific variation in glucosinolate concentrations and profiles in white cabbage cultivars. Glucosinolates, a group of circa 120 secondary plant compounds predominantly present in the Brassicaceae, have been shown to affect not only aboveground organisms but also belowground organisms. Glucosinolate profiles in both roots and shoots of white cabbage cultivars showed significant intra-specific variation. The root glucosinolate profiles were more diverse than in the shoots. The variation in root glucosinolate profiles between four of the cultivars was used to evaluate the effects of glucosinolates on a range of soil organisms from different trophic levels, which differ in their degree of association with plant roots. In the field I recorded that plant-parasitic nematodes were affected by the differences in the root glucosinolate profiles, whereas non-target organisms were not. The latter observation might be explained by the reduced intra-specific variation in the glucosinolate profiles of the root exudates compared to those of the roots. Even though total glucosinolate concentrations in roots and root exudates correlated positively, the number of individual glucosinolates that were recorded in the root exudates did not match those found in the roots. My experiments show that this may be due to different degradation rates of the individual glucosinolates in the soil.        
By adding different soil communities to sterilized soils I examined whether belowground organisms can affect aboveground organisms via their shared host plant. For this, I used two cabbage cultivars that were highly divergent both in their effects on soil organisms and glucosinolate profiles. Microorganisms added to the soils promoted aphid population growth. The addition of nematodes tended to decrease aphid population growth. However, the effect of the soil organisms on aboveground organisms was similar for both cultivars, indicating that the outcome of below-aboveground interactions was not affected by intra-specific differences.          
Genetic modification of plants could also indirectly affect plant growth, for example if the modification would affect the soil communities associated with the plants, which could subsequently affect aerial plant parts and aboveground processes. I explored this possibility by reviewing the recent literature on genetic modified plants, focusing on two case studies; rice plants modified to tolerate drought and salt stress and plants transformed to enhance their capacity to accumulate pollutants. Indeed, feedback loops between plants and the rhizosphere can result in both positive and negative feedback effects of the modified gene on aboveground plant properties. This may have unexpected consequences for the net effect of the genetic modification and eventually annihilate the positive effect of the modification on desired plant properties such as yield.               
In this thesis I also showed that when evaluating genetically modified plants in greenhouse studies, effects on soil organisms are limited when compared to the field. I propose that this is due to the fact that greenhouse studies use relatively simple soils that lack the complex plant-soil interactions that can be present in the field. This is an indication that greenhouse studies have a limited predictive value for field effects on soil organisms. Greenhouse studies are nevertheless useful for selecting a suitable and manageable set of varieties that are representative for the range of variation present in the full set of available cultivars. The selection of this sub-set can be made using the appropriate statistical tools, such as multivariate statistics. The selected sub-set can then be used as a baseline for more extensive studies assessing effects on (non-target) organisms in the field. I found that for root glucosinolate profiles this was a useful approach. Whether this holds true for other traits is yet to be assessed.
Before one can evaluate whether effects of genetically modified plants fall within or outside the effects of conventional plants, a good knowledge of the range of effects that can be observed for conventional varieties is required. In this thesis, I have provided the basis for this knowledge for white cabbage, especially for belowground interactions and to some extent on belowground-aboveground interactions. Conventional varieties already differ in their effects on soil organisms and these effects can potentially result in altered below-aboveground interactions, as was simulated by the addition of specific organism groups to the soil. This range of effects can serve as a baseline to determine whether effects of genetically modified white cabbage plants fall inside or outside the range of effects that can be observed for these conventional varieties.

Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • Wageningen University
Supervisors/Advisors
  • van der Putten, Wim, Promotor
  • van Dam, N.M., Promotor, External person
  • Biere, A., Co-promotor, External person
Award date1 Feb 2012
Place of PublicationS.l.
Publisher
Print ISBNs9789461731197
Publication statusPublished - 2012

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Keywords

  • brassica oleracea var. capitata
  • glucosinolates
  • exudates
  • genetic variation
  • genetic engineering
  • soil flora
  • soil fauna
  • nontarget organisms
  • rhizosphere
  • transgenic plants

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