The Differential Growth Inhibition of Phytophthora spp. Caused by the Rare Sugar Tagatose Is Associated With Species-Specific Metabolic and Transcriptional Changes

Abstract

Tagatose is a rare sugar with no negative impacts on human health and selective inhibitory effects on plant-associated microorganisms. Tagatose inhibited mycelial growth and negatively affected mitochondrial processes in Phytophthora infestans, but not in Phytophthora cinnamomi. The aim of this study was to elucidate metabolic changes and transcriptional reprogramming activated by P. infestans and P. cinnamomi in response to tagatose, in order to clarify the differential inhibitory mechanisms of tagatose and the species-specific reactions to this rare sugar. Phytophthora infestans and P. cinnamomi activated distinct metabolic and transcriptional changes in response to the rare sugar. Tagatose negatively affected mycelial growth, sugar content and amino acid content in P. infestans with a severe transcriptional reprogramming that included the downregulation of genes involved in transport, sugar metabolism, signal transduction, and growth-related process. Conversely, tagatose incubation upregulated genes related to transport, energy metabolism, sugar metabolism and oxidative stress in P. cinnamomi with no negative effects on mycelial growth, sugar content and amino acid content. Differential inhibitory effects of tagatose on Phytophthora spp. were associated with an attempted reaction of P. infestans, which was not sufficient to attenuate the negative impacts of the rare sugar and with an efficient response of P. cinnamomi with the reprogramming of multiple metabolic processes, such as genes related to glucose transport, pentose metabolism, tricarboxylic acid cycle, reactive oxygen species detoxification, mitochondrial and alternative respiration processes. Knowledge on the differential response of Phytophthora spp. to tagatose represent a step forward in the understanding functional roles of rare sugars.

D-Tagatose-Based Product Triggers Sweet Immunity and Resistance of Grapevine to Downy Mildew, but Not to Gray Mold Disease

“…In recent years, some rare monosaccharides and their derivatives have shown potential functional and ecological properties in controlling plant pathogens [ 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 ]. Their availability has been achieved through the implementation of new enzymatic and microbial processes, making their use effective in food and agricultural sectors [ 25 , 30 ].…”

“…D-tagatose, as a ketohexose, is among rare sugars found at low concentrations in many foods and generally recognized as safe by the Food and Drug Administration [ 30 ]. D-tagatose was shown to inhibit the growth of various plant pathogens, such as Phytophthora infestans causing late blight [ 24 ], Oidium violae causing powdery mildew in tomato [ 33 ], Plasmopara viticola (downy mildew) and Erysiphe necator (powdery mildew) in grapevine [ 32 , 33 ] and Hyaloperonospora parasitica (downy mildew) in Chinese cabbage [ 31 ]. It has been reported that D-tagatose acted directly on the pathogen by inhibiting essential enzymes leading to impairment of the whole metabolism [ 31 ].…”

Potential of Prebiotic D-Tagatose for Prevention of Oral Disease

“…In support of those findings, previous reports have noted that D-tagatose caused species-specific growth inhibition of Phytophthora spp. and decreased amino acid content in Phytophthora infestans (Chahed et al, 2020;Chahed et al, 2021). In S. oralis, the polar amino acid transporter gene (SOR_1115) was up-regulated, whereas SMU_1179c and SGO_1037, orthologous genes of SOR_1115, were down-regulated.…”

A review of knowledge on the mechanisms of action of the rare sugard‐tagatose against phytopathogenic oomycetes

“…The alterations of mitochondrial processes found in P . infestans incubated with d ‐tagatose (Chahed et al, 2020) are associated with sugar metabolism inhibition (Chahed et al, 2021; Corneo et al, 2021b; Mochizuki et al, 2020). In particular, H .…”

“…aureus , Pseudomonas aeruginosa , and Yersinia enterocolitica (Bautista et al, 2000), indicating antinutritional properties on specific microbial taxa. Likewise, d ‐tagatose inhibits the growth of some phytopathogens and it has been proposed as a promising plant protection product (Chahed et al, 2020, 2021; Corneo et al, 2021b; Mijailovic et al, 2021; Mochizuki et al, 2020; Perazzolli et al, 2020). The aim of this review is to summarize the current knowledge on the modes of action of d ‐tagatose against phytopathogenic oomycetes and to propose further functional studies that will support the use of this rare sugar for sustainable crop protection.…”