Living the Sweet Life: How Does a Plant Pathogenic Fungus Acquire Sugar from Plants?

Plant diseases are an important constraint on worldwide crop production, accounting for losses of 10–30% of the global harvest each year [1]. As a consequence, crop diseases represent a significant threat to ensuring global food security. To feed the growing human population it will be necessary to double food production by 2050, which will require the sustainable intensification of world agriculture in an era of unpredictable climate change [2,3]. Controlling the most important plant diseases represents one of the best means of delivering as much of the current productivity of crops as possible. To accomplish this task, a fundamental understanding of the biology of plant infection by disease-causing agents, such as viruses, bacteria, and fungi will be necessary [1,2]. Fungal pathogens can broadly be divided into two groups—the biotrophs and necrotrophs [4,5]. Biotrophic pathogens are parasites that have evolved the means to grow within living plant cells without stimulating plant defence mechanisms [6]. This means that they are able to spread rapidly throughout plant tissue while, at the same time, diverting nutrients from the living plant to fuel their own growth at the expense of plant productivity. In contrast, the necrotrophic pathogens use toxins and depolymerising enzymes to kill and degrade plant cells, consuming the resulting products [7]. These modes of nutrition are highly distinctive and plants have evolved independent defence mechanisms to contend with such different pathogens [5,7]. To compound this challenge to plants, some pathogens exhibit both types of nutrition, switching from biotrophic growth to a rapid killing of plant cells as disease symptoms occur [7–9]. Because of their rather sophisticated nature, biotrophic pathogens cause some of the most pervasive plant diseases, which are difficult to control. Powdery mildew of barley caused by Blumeria graminis, for instance, continues to be one of the most important temperate cereal diseases [10], while yellow and brown rust diseases cause significant losses to worldwide wheat production [11]. The spread of the UG99 strain of wheat stem rust, which is highly virulent against most elite cultivars of wheat grown around the world, throughout Africa and the Middle East, shows how vulnerable existing cereal production is to attack by these sophisticated plant parasites [12]. In order to grow, a plant pathogenic fungus must secure an organic carbon source from the plant. In most plant diseases, however, we have little idea of what constitutes the major carbon source for an invading fungus during growth in plant tissue. Fungi are osmotrophic organisms, which means that they proliferate in a substrate by secreting a large diversity of extracellular enzymes that depolymerise polymers, such as cellulose, lignin, proteins, and lipids and then deliver the resulting simple sugars, amino acids, and fatty acids into fungal hyphae by means of plasma membranelocalised transporters [8,13]. It is clear from analysing the genome sequences of both plant pathogenic and free-living fungi that they possess large numbers of extracellular enzymes and transporterencoding genes, although, as might be expected, extracellular enzymes appear more restricted in number in biotrophic species [14]. The transporters, which are of the major facilitator transporter family, allow fungi to grow on an extremely diverse set of materials and are one of the reasons why fungi can occupy such a large number of ecological niches. How do biotrophic plant pathogens acquire nutrients efficiently from a living plant cell? To understand this process it is essential to understand how plant pathogenic fungi enter living plant tissue. A large number of plant pathogenic fungal species develop specialised cells called appressoria that are able to breach the outer cuticle of plants and thereby gain entry to epidermal cells [8,9]. The plant cells are not ruptured in this process, but instead the fungus is able to invaginate the plant plasma membrane and grow within the apoplast—the space between the plant plasma membrane and the plant cell wall [13]. This allows the fungus to occupy intact, living plant cells and set up a specialised interface to allow sequestration of nutrients directly from host cells [13]. A study published in this issue of PLoS Biology [15] provides a significant advance in understanding the mechanism by which a plant pathogenic fungus is able to acquire nutrients in planta. Ustilago maydis is a biotrophic pathogen which causes corn smut—a disease that is characterised by production of tumours on the stems and leaves of maize plants and, ultimately, by the liberation of large numbers of black teliospores that allow the fungus to be disseminated to new maize plants [16]. Corn smut can be a serious disease in maize-growing regions of Mexico and the United States [16]. In the study, the authors identified a novel plasma membrane-localised sucrose transporter encoded by the SRT1 gene, and have shown its contribution to fungal virulence. SRT1 encodes a plasma membrane protein with 12 membrane-spanning domains and is unusual because, in contrast to the relatively broad spectrum hexose transporters previously identified and characterised in fungi, Srt1 appears to be specific for the transport of sucrose. The conclusions of this study are that sucrose, which constitutes the most abundant storage sugar within plants and the product of photosynthesis, is directly utilised by invading pathogens without the need for its extra-cellular degradation by fungal secreted invertases. The authors present a number of independent lines of evidence to support these conclusions. Srt1 was expressed in the yeast Saccharomyces cerevisiae, where they were able to study both its