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ARS Home » Midwest Area » Columbia, Missouri » Plant Genetics Research » Research » Publications at this Location » Publication #300158
Title: Induced carbon reallocation and compensatory growth as root herbivore tolerance mechanisms

Author
item ROBERT, CHRISTELLE - Max Planck Institute For Biogeochemistry
item FERRIERI, RICHARD - Brookhaven National Laboratory
item SCHIRMER, STEFANIE - Brookhaven National Laboratory
item BABST, BENJAMIN - Brookhaven National Laboratory
item SCHUELLER, MICHAEL - Brookhaven National Laboratory
item MACHADO, RICARDO - Max Planck Institute For Biogeochemistry
item ARCE, CARLA - Max Planck Institute For Biogeochemistry
item Hibbard, Bruce
item GERSHENZON, JONATHAN - Max Planck Institute For Biogeochemistry
item TURLINGS, TED - University Of Neuchatel
item ERB, MATTHIAS - Max Planck Institute For Biogeochemistry

Submitted to: Plant Cell and Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/5/2014
Publication Date: 11/1/2014
Publication URL: http://handle.nal.usda.gov/10113/59884
Citation: Robert, C.A., Ferrieri, R.A., Schirmer, S., Babst, B.A., Schueller, M.J., Machado, R.A., Arce, C.C., Hibbard, B.E., Gershenzon, J., Turlings, T.C., Erb, M. 2014. Induced carbon reallocation and compensatory growth as root herbivore tolerance mechanisms. Plant Cell and Environment. 37:2613-2622.

Interpretive Summary: When fed upon by leaf-herbivores, plants reallocate sugar and related carbon resources to the roots. It has been suggested that this response to insect feeding is a tolerance response, as the carbon resources stored in below ground tissues may be used for later regrowth. How plants react with carbon resources when the roots are fed upon by insects has been poorly understood. We investigated this aspect by using a radioactive isotope of carbon dioxide with a half-life of just more than 20 hours and detectors that are highly sensitive to radiation. We demonstrated that corn plants that are being fed upon by the western corn rootworm allocate more carbon from leaves to stems, not roots. The induced aboveground carbon reallocation was associated with increased growth of stem-borne roots in induced plants following herbivore removal, suggesting that retaining the carbon in the shoots may help root-attacked plants to compensate for root tissue loss. The increased capacity for regrowth was found to be independent of the plant’s water supply. Starch concentrations were significantly reduced in the roots but did not consistently increase in the shoots, indicating a role for other carbon storage forms in the observed tolerance phenomenon. These data add important basic information on how corn plants tolerate damage from its most important pest.

Technical Abstract: Upon attack by leaf-herbivores, many plants reallocate photoassimilates below ground. However, little is known about how plants respond when the roots themselves come under attack. We investigated this aspect in maize seedlings infested by the specialist root herbivore Diabrotica virgifera. By using radioactive 11CO2 in combination with autoradiography and gamma counting of tissue sections, we demonstrate that root-attacked maize plants allocate more new 11C carbon from source leaves to stems, but not to roots. Reduced meristematic activity and reduced invertase activity in attacked maize root systems are identified as possible drivers of the reallocation response. The increased allocation of photoassimilates to stems is shown to be associated with a marked thickening of these tissues and increased growth of stem-borne crown roots in induced plants. The strong quantitative correlation between stem thickness and root re-growth across different watering levels suggests that retaining the carbon in the shoots may help root-attacked plants to compensate for the loss of below ground tissues. Taken together, our results indicate that induced tolerance may be an important strategy of plants to withstand below ground attack. Furthermore, root-herbivore induced carbon reallocation needs to be taken into account when studying plant-mediated interactions between herbivores.