Proteomics 2013, 13, 597–608 597 DOI 10.1002/pmic.201200282 REVIEW Secretomes: The fungal strike force Vincent Girard, Cindy Dieryckx, Claudette Job and Dominique Job ∗ Bayer CropScience Joint Laboratory (UMR5240), CNRS, University Lyon1, Lyon, France Microorganisms, although being very diverse because they comprise prokaryotic organisms such as bacteria or eukaryotic organisms such as fungi, all share an essential exodigester func- tion. The consequence is their essential need to have a secretome adapted to their environment. The selection pressure exerted by environmental constraints led to the emergence of species with varying complexity in terms of composition of their secretomes. This review on fungal secretomes highlights the extraordinary variability among these organisms, even within the same species, and hence the absolute necessity to fully characterize all their components in the aims of understanding the fundamental mechanisms responsible for secretome plasticity and developing applications notably toward a better control of diseases caused by these pathogens. Keywords: Microorganisms / Secretomes / Secretomic variability and adaptability Received: July 6, 2012 Revised: October 1, 2012 Accepted: October 5, 2012 1 Introduction 1.1 Preamble: Definition of secretome In 2000 Tjalsma et al. [1] coined the term “secretome” in their study of the eubacterium Bacillus subtilis. They defined the se- cretome as all of the secreted proteins and secretory machin- ery of the bacteria. Depending on the authors, this secretome protein population includes any protein strictly external to the plasma membrane or includes only the soluble proteins at the exterior of the cell wall. In 2010, Agrawal et al. [2] sug- gested defining the secretome as “the global group of secreted proteins into the extracellular space by a cell, tissue, organ, or organism at any given time and conditions through known and unknown secretory mechanisms involving constitutive and regulated secretory organelles.” The high capacity of the secretion machinery of filamen- tous fungi has been widely exploited for the production of homologous and heterologous proteins [3]. However, our knowledge of the fungal secretion pathway is still at an early Correspondence: Dr. Vincent Girard, CNRS/UCBL/Bayer Crop- Science Joint Laboratory (UMR CNRS 5240), 14, impasse Pierre Baizet, F-69263, Lyon cedex 09, France E-mail: vincent.girard@bayer.com Fax: +33-4-72-85-22-80 Abbreviations: 2DE, 2D electrophoresis; EPs, extracellular polysaccharides; LSP, leaderless secretory protein; PKS, polyke- tide synthetase; SRM, selected reaction monitoring; SSP, small secreted protein stage. Most of this knowledge comes from models developed in yeasts and higher eukaryotes, which have served as refer- ences for the studies on fungal species. Here, we discuss the exhaustive data accumulated in recent years on proteomics of fungal secretion [3], notably with respect to the interactions between plants and fungi. 1.2 Higher plant versus fungal secretomes The most important difference between plants and fungi is that plants are able to synthesize their own food, while fungi cannot. This is because that for this purpose plants can use through photosynthesis carbon dioxide, sunlight, and water. In contrast, fungi usually eat off their hosts as parasites or de- compose matter and take it as their food. Accordingly, plants and fungi play different roles in the whole ecological sys- tem. Thus, plants are predominantly considered as being producers, owing to their capacity to produce food. The role of fungi is just the opposite. They are the decomposers that break down biomass. Imagine what this earth would be with- out such busy cleaners—just a large dustbin that was never cleaned out! ∗ Additional corresponding author: Dr. Dominique Job, E-mail: dominique.job@bayer.com Colour Online: See the article online to view Fig. 1 in colour. C 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.proteomics-journal.com