TY - JOUR

T1 - Metabolic control of tobacco pollination by sugars and invertases

AU - Goetz, Marc

AU - Guivarc'h, Anne

AU - Hirsche, Jörg

AU - Bauerfeind, Martin Andreas

AU - González, María-Cruz

AU - Hyun, Tae Kyung

AU - Eom, Seung Hee

AU - Chriqui, Dominique

AU - Engelke, Thomas

AU - Grosskinsky, Dominik Kilian

AU - Roitsch, Thomas Georg

PY - 2017

Y1 - 2017

N2 - Pollination in flowering plants is initiated by germination of pollen grains on stigmas followed by fast growth of pollen tubes representing highly energy-consuming processes. The symplastic isolation of pollen grains and tubes requires import of sucrose available in the apoplast. We show that the functional coupling of sucrose cleavage by invertases and uptake of the released hexoses by monosaccharide transporters are critical for pollination in tobacco. Transcript profiling, in situ hybridization and immunolocalization of extracellular invertases and two monosaccharide transporters in vitro and in vivo support the functional coupling in supplying carbohydrates for pollen germination and tube growth evidenced by spatiotemporally coordinated expression. Detection of vacuolar invertases in maternal tissues by these approaches revealed metabolic cross-talk between male and female tissues and supported the requirement for carbohydrate supply in transmitting tissue during pollination. Tissue-specific expression of an invertase inhibitor and addition of the chemical invertase inhibitor miglitol strongly reduced extracellular invertase activity and impaired pollen germination. Measurements of (competitive) uptake of labelled sugars identified two import pathways for exogenously available sucrose into the germinating pollen operating in parallel: direct sucrose uptake and via the hexoses after cleavage by extracellular invertase. Reduction of extracellular invertase activity in pollen decreases sucrose uptake and severely compromises pollen germination. We further demonstrate that glucose as sole carbon source is sufficient for pollen germination, whereas sucrose is supporting tube growth, revealing an important regulatory role of both the invertase substrate and products contributing to a potential metabolic and signaling-based multilayer regulation of pollination by carbohydrates.

AB - Pollination in flowering plants is initiated by germination of pollen grains on stigmas followed by fast growth of pollen tubes representing highly energy-consuming processes. The symplastic isolation of pollen grains and tubes requires import of sucrose available in the apoplast. We show that the functional coupling of sucrose cleavage by invertases and uptake of the released hexoses by monosaccharide transporters are critical for pollination in tobacco. Transcript profiling, in situ hybridization and immunolocalization of extracellular invertases and two monosaccharide transporters in vitro and in vivo support the functional coupling in supplying carbohydrates for pollen germination and tube growth evidenced by spatiotemporally coordinated expression. Detection of vacuolar invertases in maternal tissues by these approaches revealed metabolic cross-talk between male and female tissues and supported the requirement for carbohydrate supply in transmitting tissue during pollination. Tissue-specific expression of an invertase inhibitor and addition of the chemical invertase inhibitor miglitol strongly reduced extracellular invertase activity and impaired pollen germination. Measurements of (competitive) uptake of labelled sugars identified two import pathways for exogenously available sucrose into the germinating pollen operating in parallel: direct sucrose uptake and via the hexoses after cleavage by extracellular invertase. Reduction of extracellular invertase activity in pollen decreases sucrose uptake and severely compromises pollen germination. We further demonstrate that glucose as sole carbon source is sufficient for pollen germination, whereas sucrose is supporting tube growth, revealing an important regulatory role of both the invertase substrate and products contributing to a potential metabolic and signaling-based multilayer regulation of pollination by carbohydrates.

U2 - 10.1104/pp.16.01601

DO - 10.1104/pp.16.01601

M3 - Journal article

C2 - 27923989

VL - 173

SP - 984

EP - 997

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 2

ER -