pH Regulation of Ammonia Secretion by Colletotrichum gloeosporioides and Its Effect on Appressorium Formation and Pathogenicity

Abstract

Host-tissue alkalinization via ammonia accumulation is key to Colletotrichum spp. colonization. Using macroarrays carrying C. gloeosporioides cDNAs, we monitored gene expression during the alkalinization process. A set of genes involved in synthesis and catabolism of ammonia accumulation were identified. Expression of NAD(+)-specific glutamate dehydrogenase (GDH2, encoding ammonia synthesis) and the ammonia exporter AMET were induced at pH 4.0 to 4.5. Conversely, ammonia uptake and transcript activation of the ammonia and glutamate importers (MEP and GLT, respectively) and glutamine synthase (GS1) were higher at pH 6.0 to 7.0. Accumulated ammonia in the wild-type mycelium decreased during ambient alkalinization, concurrent with increased GS1 expression. Deltapac1 mutants of C. gloeosporioides, which are sensitive to alkaline pH changes, showed upregulation of the acid-expressed GDH2 and downregulation of the alkaline-expressed GS1, resulting in 60% higher ammonia accumulation inside the mycelium. Deltagdh2 strains of C. gloeosporioides, impaired in ammonia production, showed 85% inhibition in appressorium formation followed by reduced colonization on avocado fruit (Persea americana cv. Fuerte) pericarp, while exogenic ammonia addition restored appressoria formation. Thus the modulation of genes involved in ammonia metabolism and catabolism by C. gloeosporioides is ambient pH-dependent. Aside from its contribution to necrotrophic stages, ammonia accumulation by germinating spores regulates appressorium formation and determines the initiation of biotrophic stages of avocado-fruit colonization by Colletotrichum spp.

Entry Mode–Dependent Function of an Indole Glucosinolate Pathway in Arabidopsis for Nonhost Resistance against Anthracnose Pathogens

“…It has been reported that some Colletotrichum species, including Cg, develop lesions via mycelial inoculation on wounded surfaces of their hosts (Alkan et al, 2008;Miyara et al, 2010). It is plausible that fungal hyphae enter the hosts through these wounds.…”

Frequency of Quiescent Fungi and Post-Harvest Alternative Management of Stem End Rot in Papaya

“…The other pathogens were observed in places of injury, which is another form of penetration. It should be stressed that there are reports of several species of Lasiodiplodia and Colletotrichum surviving in a quiescent form in their hosts (YUJU et al, 2009;MYARA et al, 2010).…”

Virulence Regulation of Phytopathogenic Fungi by pH

“…The ability of the pathogen to alter the pH locally has been described initially for Sclerotinia sclerotiorum, but similar findings been have extended to some other pathogens, such as Colletotrichum spp., Alternaria alternata, Botrytis cinerea, Penicillium expansum, P. digitatum, P. italicum, Phomopsis mangiferae, and Fusarium oxysporum (39, 52, 53, 89,100,101,123,124,129). To simplify the terminology in the following discussion, fungi that alkalinize the environment will be referred to as ''alkaline fungi'' and those that acidify it will be called ''acidic fungi'' (Fig.…”

“…Ammonium accumulation has been detected in association with pathogenicity of many Colletotrichum species, including C. gloeosporioides, C. acutatum, C. higgisianum, C. graminicola, and C. coccodes (1,46,100,110); Alternaria alternata (52, 53); and Fusarium oxysporum (101). The ammonium secreted by Colletotrichum spp., F. oxysporum and A. alternata result in alkalization of the host tissue, and its concentration can reach approximately 5 mM, as found in decayed avocado, tomato, and persimmon fruits (1,52,53,100). In every case, increased ammonium accumulation has been related to enhanced pathogenicity of Colletotrichum spp.…”

“…In every case, increased ammonium accumulation has been related to enhanced pathogenicity of Colletotrichum spp. (1,2,100). Recent findings that F. oxysporum, C. graminicola, and C. higginsianum secrete ammonia (101,110) suggest that various fungal pathogens modulate the surrounding pH to create an optimal pH for expression and activity of their pathogenicity factors.…”