Multiple roles of soluble sugars in the establishment of Gunnera-Nostoc endosymbiosis.
Gunnera plants have the unique ability to form endosymbioses with N(2)-fixing cyanobacteria, primarily Nostoc. Cyanobacteria enter Gunnera through transiently active mucilage-secreting glands on stems. We took advantage of the nitrogen (N)-limitation-induced gland development in Gunnera manicata to identify factors that may enable plant tissue to attract and maintain cyanobacteria colonies. Cortical cells in stems of N-stressed Gunnera plants were found to accumulate a copious amount of starch, while starch in the neighboring mature glands was nearly undetectable. Instead, mature glands accumulated millimolar concentrations of glucose (Glc) and fructose (Fru). Successful colonization by Nostoc drastically reduced sugar accumulation in the surrounding tissue. Consistent with the abundance of Glc and Fru in the gland prior to Nostoc colonization, genes encoding key enzymes for sucrose and starch hydrolysis (e.g. cell wall invertase, α-amylase, and starch phosphorylase) were expressed at higher levels in stem segments with glands than those without. In contrast, soluble sugars were barely detectable in mucilage freshly secreted from glands. Different sugars affected Nostoc's ability to differentiate motile hormogonia in a manner consistent with their locations. Galactose and arabinose, the predominant constituents of polysaccharides in the mucilage, had little or no inhibitory effect on hormogonia differentiation. On the other hand, soluble sugars that accumulated in gland tissue, namely sucrose, Glc, and Fru, inhibited hormogonia differentiation and enhanced vegetative growth. Results from this study suggest that, in an N-limited environment, mature Gunnera stem glands may employ different soluble sugars to attract Nostoc and, once the cyanobacteria are internalized, to maintain them in the N(2)-fixing vegetative state.
Khamar
Hima J
HJ
Department of Biology, Virginia Commonwealth University, Richmond, Virginia 23284, USA.
Breathwaite
Erick K
EK
Prasse
Christine E
CE
Fraley
Elizabeth R
ER
Secor
Craig R
CR
Chibane
Fairouz L
FL
Elhai
Jeff
J
Chiu
Wan-Ling
WL
D050260:Carbohydrate Metabolism; D005632:Fructose / Q000378:metabolism; D005947:Glucose / Q000378:metabolism; D019684:Magnoliopsida / Q000235:genetics / Q000378:metabolism / Q000382:microbiology*; D046937:Nostoc / Q000378:metabolism*; D018749:RNA, Plant / Q000235:genetics; D036226:Seedlings / Q000235:genetics / Q000378:metabolism / Q000382:microbiology; D013213:Starch / Q000378:metabolism; D013559:Symbiosis
D018749:RNA, Plant; D005632:Fructose; D013213:Starch; D005947:Glucose