Frontiers in molecular mycorrhizal research – genes, loci, dots and spins

Abstract

Functional genomics is revolutionizing our understanding of biological mechanisms, nowhere more than in complex symbiotic systems. Functional genomics entails the analysis of all of the genetic material (the genome) of an organism, and then relating it to the form and function of that organism. Through the application of the cutting-edge tools of genome analysis at several levels – those of the genome, transcriptome, proteome and metabolome – remarkable progress has been made in understanding the mechanisms that control the development and functioning of nitrogen-fixing symbioses (Harrison, 1999; Downie & Bonfante, 2000; Györgyey et al., 2000). A surge of investigations based on these novel approaches (large scale gene sequencing, cDNA array analysis of gene expression, proteomics) have recently allowed an assessment of the development and functioning of arbuscular endomycorrhizal (AM) and ectomycorrhizal (ECM) symbioses (Box 1) on a larger scale (Harrison, 1999; Lapopin et al., 1999; Bago et al., 2001; Voiblet et al., 2001). Similarly, PCR-based detection of genome polymorphisms have revolutionized our perception of the ecology of mycorrhizal fungi (Peter et al., 2001). However, the limitations and ultimate utility of genomics to determine the ecological role of the mycorrhizal symbiosis in the real world remain to be determined. The reviews featured in this issue of New Phytologist have been selected with all these issues in mind. In addition to providing the ‘state-of-the-art’ of current knowledge of molecular mechanisms driving the development, physiology and ecology of the symbiosis, the reviews also provide a glimpse of things to come. Understanding the complexity of the interactions between mycorrhizal symbionts and how these mutualistic associations adapt and respond to changes in the biological, chemical and physical properties of the rhizosphere remains a significant challenge for plant and microbial biologists. Identification of the primary genetic determinants controlling the development of the symbiosis and its metabolic activity (e.g. P and N scavenging) will open the door to understanding the ecological fitness of the mycorrhizal symbiosis. The symbiosis provides an additional layer of complexity to the challenge of designing experimental systems and framing questions, and thus it has been relatively difficult to study these primary genetic determinants. For many years, most physiological analyses were focused on limited sections of the complex metabolic networks (e.g. N and P acquisition and assimilation) taking place in symbionts (Hampp et al., 1995; Harrison, 1999), which limited the degree to which symbiosis behaviour could be understood. Molecular details of mycorrhiza development and functioning are now becoming experimentally tractable owing to simultaneous advances in various fields. The molecular identity of recently discovered symbiosis-regulated (SR) genes, the analysis of mycorrhiza mutants, new experimental approaches, such as cDNA arrays, and innovative applications of older technologies, such as NMR, are together generating a conceptual framework for understanding the formation and physiology of mycorrhizas in which model predictions can now be tested at the molecular level. While familiar with the practicalities of making a PCR or a biochemical analysis, many scientists lack a ‘nuts-and-bolts’ appreciation of the pros and cons of functional genomics. Detailed and thorough understanding of the options available improves the odds that one’s choice will be vindicated; an appreciation of the biological and ecological contexts of genetic (and genomic) questions can also be critical to the success of genome-based analysis. At present, we do not know either the molecular mechanisms underlying overall symbiotic tissue patterning nor the specific signals ensuring fungus–root-coordinated development and metabolic continuity between symbiotic partners and between the different hyphal networks (i.e. Hartig n