Eco-physiological and molecular manipulation of leaf-level primary and secondary metabolism by arthropod herbivory

Nabity, Paul

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Description

Title

Eco-physiological and molecular manipulation of leaf-level primary and secondary metabolism by arthropod herbivory

Author(s)

Nabity, Paul

Issue Date

2012-09-18T21:12:09Z

Director of Research (if dissertation) or Advisor (if thesis)

DeLucia, Evan H.

Doctoral Committee Chair(s)

DeLucia, Evan H.

Committee Member(s)

• Berenbaum, May R.
• Leakey, Andrew D.
• Zielinski, Raymond E.

Department of Study

Plant Biology

Discipline

Plant Biology

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• plant-insect interactions
• photosynthesis
• defense
• stomata

Abstract

Arthropod herbivory fundamentally alters ecosystem function and challenges agricultural productivity because herbivores alter photosynthesis. Feeding removes tissues and resources for growth but often introduces unseen physiological costs mediated by a reallocation in resources from growth to defense or by alterations to primary and secondary metabolism. The type of feeding damage depends on the mouthparts of the herbivore and, in part, determines the magnitude and mechanism by which photosynthesis is altered. However, there is a lack of understanding of these effects across model systems to evaluate conserved mechanisms of plant responses to herbivory. Documenting these responses from the observed and manipulated eco-physiological level down to the level of the gene can provide mechanistic understanding of how photosynthesis changes under herbivory and, ultimately, what initiates the reallocation of resources from primary to secondary metabolism (i.e., plant defense). Understanding the connections between genotype and phenotype can enhance our knowledge of ecosystem function amidst a rapidly changing climate by elucidating resource-driven trade-offs, and, as a result, forms the basis for this dissertation. Plant responses to herbivory depend on the plant under attack and the attacking agent, but variability in the methods by which the interaction is observed makes it difficult to distinguish trends. As such, I synthesized the available literature in a review that elucidated four mechanisms for the alteration of photosynthesis at the leaf level. Arthropods sever vasculature, alter sink/source relationships, release autotoxic chemicals, or initiate a trade-off of resources from photosynthesis to defense in remaining leaf tissue. This review is presented in Chapter 2 and establishes the framework for the following chapters in which I investigate these mechanisms. Because Earth is experiencing rapid environmental change, I surveyed leaf-level response of model forest species to multiple damage types when grown under predicted climate change conditions in Chapter 3. Elevated CO2 attenuated damage for all damage types. As a result, the changing climate will, in part, attenuate the negative effects of herbivory on leaf-level photosynthesis. A common theme in this study and others is that damage to remaining leaf tissue from defoliation declines with time across species; however, contrary examples exist where inducible processes interact more with photosynthesis. Therefore I examined how inducible defense signaling and metabolite production altered photosynthesis in Chapter 4. I found that wound signaling immediately impaired electron transport, and defense synthesis correlated with sustained reductions in photosynthesis. Taken together, these data indicate a conserved mechanism underlying defense signaling modulates the trade-off from using resources for growth to defense. As the preceding chapters suggest, hidden physiological costs can reduce photosynthesis relative to the damage type. Insect parasites of plants may influence leaf and canopy-level processes through the manipulation of sink/source dynamics by an unknown mechanism. In Chapter 5 I reexamined the grape-phylloxera system to reveal that the gall-forming insect parasite phylloxera induces functional stomata and globally reconfigures plant metabolism at the genomic level to enhance insect fitness. Although insect-induced stomata are rare in nature, the transcriptional pattern of gall formation is likely conserved among insect parasites and facilitates the galling habit by increasing competitive sink strength of the insect. The following chapters provide a framework for assessing how arthropod herbivores alter leaf function across damage type and plant species. By characterizing mechanisms within model systems, I believe I have uncovered some of the physiological costs of herbivory that modulate resource-driven trade-offs in nature.

Graduation Semester

2012-08

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Copyright and License Information

Copyright 2012 Paul Nabity

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