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Modification of esterified cell wall phenolics increases vulnerability of tall fescue to herbivory by the fall armyworm

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Abstract

Feruloylation of arabinoxylan in grass cell walls leads to cross-linked xylans. Such cross-linking appears to play a role in plant resistance to pathogens and insect herbivores. In this study, we investigated the effect of ferulate cross-linking on resistance to herbivory by fall armyworm (Spodoptera frugiperda) making use of genetically modified tall fescue [Schedonorus arundinaceus (Festuca arundinacea)] expressing a ferulic acid esterase gene. Mature leaves of these plants have significant reduced levels of cell wall ferulates and diferulates but no change in acid detergent lignin. These reduced levels of esterified cell wall ferulates in transgenic plants had a positive effect on all measures of armyworm larval performance examined. More larvae survived (89 vs. 57 %) and grew faster (pupated 2.1 days sooner) when fed transgenic leaves with reduced levels of cell wall ferulates, than when fed control tall fescue leaves where levels of cell wall ferulates were not altered. Overall, mortality, growth and food utilization were negatively associated with level of esterified cell wall ferulates and diferulates in leaves they were fed. This study is the first to use transgenic plants with modified level of cell wall esterified ferulates to test the role of feruloylation in plant resistance to insects. It is concluded that the accumulation of ferulates and the cross-linking of arabinoxylans via diferulate esters in the leaves of tall fescue underlies the physical barrier to insect herbivory. Reducing ferulate cross-linking in grass cell walls could increase susceptibility of these plants to insect folivores.

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Abbreviations

AX:

Arabinoxylan

GAX:

Glucuronoarabinoxylan

FA:

Ferulic acid

HCA:

Hydroxycinnamic acid

FAW:

Fall armyworm

FAEA:

Ferulic acid esterase

AD:

Approximate digestibility

ECI:

Efficiency of conversion of ingested food

ECD:

Efficiency of conversion of digested food into biomass

RGR:

Relative growth rate

GLM:

General linear model

SE:

Standard error

tFA:

Trans-ferulic acid

cFA:

cis-ferulic acid

tpCA:

Trans p-coumaric acid

5-5′ DFA:

5-5′-diferulic acid

8-0-4′ DFA:

8-0-4′-diferulic acid

8-5C DFA:

8-5cyc diferulic acid benzofuran

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Acknowledgments

Authors’ acknowledge the National Research Initiative or Agriculture and Food Research Initiative Competitive Grants Program grant No. 2008-02863 from the USDA National Institute of Food and Agriculture, for funding. We thank IBERS (Institute of Biological, Environmental and Rural Sciences) at Aberystwyth University, UK for permission to use the plant material in the current work, Robert Meagher for providing eggs of the rice strain, and James Marden for statistical consultation and allowing HWF to perform experiments involving insects in his laboratory and environmental chamber. Additional support for HWF was from the NSF IOS Grant No. 0950416.

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  1. Department of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park, PA, 16802, USA

    Marcia M. de O. Buanafina & Howard W. Fescemyer

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  1. Marcia M. de O. Buanafina
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  2. Howard W. Fescemyer
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Correspondence to Marcia M. de O. Buanafina.

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Buanafina, M.M.O., Fescemyer, H.W. Modification of esterified cell wall phenolics increases vulnerability of tall fescue to herbivory by the fall armyworm. Planta 236, 513–523 (2012). https://doi.org/10.1007/s00425-012-1625-y

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