Hexose Transporters of a Hemibiotrophic Plant Pathogen

Abstract

Plant pathogenic fungi use a wide range of different strategies to gain access to the carbon sources of their host plants. The hemibiotrophic maize pathogen Colletotrichum graminicola (teleomorph Glomerella graminicola) colonizes its host plants, and, after a short biotrophic phase, switches to destructive, necrotrophic development. Here we present the identification of five hexose transporter genes from C. graminicola, CgHXT1 to CgHXT5, the functional characterization of the encoded proteins, and detailed expression studies for these genes during vegetative and pathogenic development. Whereas CgHXT4 is expressed under all conditions analyzed, transcript abundances of CgHXT1 and CgHXT3 are transiently up-regulated during the biotrophic phase, and CgHXT2 and CgHXT5 are expressed exclusively during necrotrophic development. Analyses of the encoded proteins characterized CgHXT5 as a low-affinity/highcapacity hexose transporter with a narrow substrate specificity for glucose and mannose. In contrast, CgHXT1 to CgHXT3 are high affinity/low capacity transporters that also accept other substrates, including fructose, galactose, or xylose. CgHXT4, the largest of the identified proteins, has only little transport activity and may function as a sugar sensor. Phylogenetic studies revealed hexose transporters closely related to the five CgHXT proteins also in other pathogenic fungi suggesting conserved functions of these proteins during fungal pathogenesis.The ascomycete Colletotrichum graminicola (Cesati) Wilson [teleomorph Glomerella graminicola (Politis)] is the causal agent of the worldwide occurring stem rot and leaf anthracnose of maize (Zea mays). Its hemibiotrophic lifestyle is characterized by an enduring destructive (necrotrophic) development that follows a short non-destructive (biotrophic) period of primary invasion and colonization (1, 2). The primary hyphae formed during this initial biotrophic phase invaginate but do not breach the plasma membrane of the host, as C. graminicola still depends on living host cells for an efficient transfer of nutrients (3). During the necrotrophic phase, however, which is initiated 48 to 72 h postinoculation, fast growing thin secondary hyphae breach the plant plasma membrane, kill the cell, and start to ramify within the host tissue. At the same time, secreted enzymes (4) degrade plant extracellular polysaccharides releasing a variety of mono-, di-, and oligosaccharides that are immediately accessibly for the fungus. Obviously, the fungus will need to respond to the changing carbon environment during these infection stages, to establish different transport systems in its plasma membrane, and to adjust the uptake of organic carbon sources to the changing concentrations and composition of its environment.So far, nothing is known about the carbon sources used by C. graminicola or other hemibiotrophic fungi at these different infection stages or about the transport proteins used for carbon acquisition in infected plant material. However, over the last years plasma membrane-localiz...

Transcriptome Profiling of the Phaseolus vulgaris - Colletotrichum lindemuthianum Pathosystem

“…These genes are necessary for the defense response, whereas at 72 hpi most of these genes were down-regulated, which probably resulted in the development of disease and eventual necrotrophy. Similar to the data presented herein, the differential expression of sugar transporters during the necrotrophic phase have also been reported to be crucial for pathogenesis [63, 64, 65, 66]. …”

“…At this phase various sugar breaking enzymes have been reported to be crucial for the survival of fungus in the necrotic lesion [67, 68, 69]. To cope with less carbon, the up regulation of genes for sugar transporters which have different substrate specificities represents a key factor in the development of the pathogen within its host [63, 65]. Host driven restrictions of nutritional compounds might be significant contributors of disease resistance in the resistant NIL.…”

Identification and characterization of the glucose dual-affinity transport system in Neurospora crassa: pleiotropic roles in nutrient transport, signaling, and carbon catabolite repression

“…Except for U. maydis , most tested fungal species possessed a homolog of GLT-1 and one or two HGTs. For example, several functionally identified low- and high-affinity glucose transporters (MstE, MstC/HxtE, and HxtC in A. nidulans [60–62]; MstE, MstA, and MstH in A. niger [63, 64]; and CgHXT5, CgHXT3, and CgHXT1 in C. graminicola [65]) were clustered into the respective GLT-1, HGT-1, and HGT-2 groups (Fig. 11), suggesting robust conservation of this dual-affinity transport system in the kingdom Fungi.…”

Gene Expression and Silencing Studies in Phytophthora infestans Reveal Infection-Specific Nutrient Transporters and a Role for the Nitrate Reductase Pathway in Plant Pathogenesis

“…Such genes are possibly wired into regulatory networks that respond to multiple biosubstances or developmental cues. A link to development has been suggested for some transporter genes in fungi, where some family members have similar substrate specificities and K m values yet are expressed at distinct stages of the life cycle [57], or have acquired additional roles in regulating metabolism [58]. …”