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J. Biol. Chem., Vol. 279, Issue 1, 429-435, January 2, 2004

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Targeted Gene Disruption of Glycerol-3-phosphate Dehydrogenase in Colletotrichum gloeosporioides Reveals Evidence That Glycerol Is a Significant Transferred Nutrient from Host Plant to Fungal Pathogen^*

Yangdou Wei, Wenyun Shen¶, Melanie Dauk¶, Feng Wang, Gopalan Selvaraj¶, and Jitao Zou¶||

From the ^¶Plant Biotechnology Institute, National Research Council of Canada, Saskatoon, Saskatchewan S7N OW9, Canada and the Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5E2, Canada

Unidirectional transfer of nutrients from plant host to pathogen represents a most revealing aspect of the parasitic lifestyle of plant pathogens. Whereas much effort has been focused on sugars and amino acids, the identification of other significant metabolites is equally important for comprehensive characterization of metabolic interactions between plants and biotrophic fungal pathogens. Employing a strategy of targeted gene disruption, we generated a mutant strain (gpdh) defective in glycerol-3-phosphate dehydrogenase in a hemibiotrophic plant pathogen, Colletotrichum gloeosporioides f.sp. malvae. The gpdh strain had severe defects in carbon utilization as it could use neither glucose nor amino acids for sustained growth. Although the mutant mycelia were able to grow on potato dextrose agar medium, they displayed arrhythmicity in growth and failure to conidiate. The metabolic defect of gpdh could be entirely ameliorated by glycerol in chemically defined minimal medium. Furthermore, glycerol was the one and only metabolite that could restore rhythmic growth and conidiation of gpdh. Despite the profound defects in carbon source utilization, in planta the gpdh strain exhibited normal pathogenicity, proceeded normally in its life cycle, and produced abundant conidia. Analysis of plant tissues at the peripheral zone of fungal infection sites revealed a time-dependent reduction in glycerol content. This study provides strong evidence for a role of glycerol as a significant transferred metabolite from plant to fungal pathogen.

Received for publication, July 3, 2003 , and in revised form, October 15, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY331190.

^* This work was supported in part by the National Research Council of Canada core program (to J. Z.) and grants from the Natural Sciences and Engineering Research Council of Canada and the Canada Foundation for Innovation (to Y. W.). This is National Research Council of Canada publication number 45273. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence may be addressed. Tel.: 306-966-4447; Fax: 306-975-4839; E-mail: yangdou.wei{at}usask.ca. || To whom correspondence may be addressed. E-mail: jitao.zou{at}nrc-cnrc.gc.ca.

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