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Microbial Volatile-Induced Accumulation of Exceptionally High Levels of Starch in Arabidopsis Leaves Is a Process Involving NTRC and Starch Synthase Classes III and IV

October 2011 , Volume 24 , Number  10
Pages  1,165 - 1,178

Jun Li,1 Ignacio Ezquer,1 Abdellatif Bahaji,1,2 Manuel Montero,1 Miroslav Ovecka,1,3 Edurne Baroja-Fernández,1 Francisco José Muñoz,1 Ángel Mérida,4 Goizeder Almagro,1 Maite Hidalgo,1 María Teresa Sesma,1 and Javier Pozueta-Romero1

1Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra). Mutiloako etorbidea z/g, 31192 Mutiloabeti, Nafarroa, Spain; 2Iden Biotechnology S.L., Av. Conde Oliveto 2, 3I, 31002 Pamplona, Nafarroa, Spain; 3Institute of Botany, Slovak Academy of Sciences, Dubravska cesta 9, SK-84523 Bratislava, Slovakia; 4Instituto de Bioquímica Vegetal y Fotosíntesis. CSIC-US. Avda Américo Vespucio, 49. 41092-Sevilla, Spain

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Accepted 1 June 2011.

Microbial volatiles promote the accumulation of exceptionally high levels of starch in leaves. Time-course analyses of starch accumulation in Arabidopsis leaves exposed to fungal volatiles (FV) emitted by Alternaria alternata revealed that a microbial volatile-induced starch accumulation process (MIVOISAP) is due to stimulation of starch biosynthesis during illumination. The increase of starch content in illuminated leaves of FV-treated hy1/cry1, hy1/cry2, and hy1/cry1/cry2 Arabidopsis mutants was many-fold lower than that of wild-type (WT) leaves, indicating that MIVOISAP is subjected to photoreceptor-mediated control. This phenomenon was inhibited by cordycepin and accompanied by drastic changes in the Arabidopsis transcriptome. MIVOISAP was also accompanied by enhancement of the total 3-phosphoglycerate/Pi ratio, and a two- to threefold increase of the levels of the reduced form of ADP-glucose pyrophosphorylase. Using different Arabidopsis knockout mutants, we investigated the impact in MIVOISAP of downregulation of genes directly or indirectly related to starch metabolism. These analyses revealed that the magnitude of the FV-induced starch accumulation was low in mutants impaired in starch synthase (SS) classes III and IV and plastidial NADP-thioredoxin reductase C (NTRC). Thus, the overall data showed that Arabidopsis MIVOISAP involves a photocontrolled, transcriptionally and post-translationally regulated network wherein photoreceptor-, SSIII-, SSIV-, and NTRC-mediated changes in redox status of plastidial enzymes play important roles.

© 2011 The American Phytopathological Society