Spatio-temporal relief from hypoxia and production of reactive oxygen species during bud burst in grapevine (Vitis vinifera).
OBJECTIVE
Plants regulate cellular oxygen partial pressures (pO2), together with reduction/oxidation (redox) state in order to manage rapid developmental transitions such as bud burst after a period of quiescence. However, our understanding of pO2 regulation in complex meristematic organs such as buds is incomplete and, in particular, lacks spatial resolution.


METHODS
The gradients in pO2 from the outer scales to the primary meristem complex were measured in grapevine (Vitis vinifera) buds, together with respiratory CO2 production rates and the accumulation of superoxide and hydrogen peroxide, from ecodormancy through the first 72 h preceding bud burst, triggered by the transition from low to ambient temperatures.


RESULTS
Steep internal pO2 gradients were measured in dormant buds with values as low as 2·5 kPa found in the core of the bud prior to bud burst. Respiratory CO2 production rates increased soon after the transition from low to ambient temperatures and the bud tissues gradually became oxygenated in a patterned process. Within 3 h of the transition to ambient temperatures, superoxide accumulation was observed in the cambial meristem, co-localizing with lignified cellulose associated with pro-vascular tissues. Thereafter, superoxide accumulated in other areas subtending the apical meristem complex, in the absence of significant hydrogen peroxide accumulation, except in the cambial meristem. By 72 h, the internal pO2 gradient showed a biphasic profile, where the minimum pO2 was external to the core of the bud complex.


CONCLUSIONS
Spatial and temporal control of the tissue oxygen environment occurs within quiescent buds, and the transition from quiescence to bud burst is accompanied by a regulated relaxation of the hypoxic state and accumulation of reactive oxygen species within the developing cambium and vascular tissues of the heterotrophic grapevine buds.
School of Plant Biology, and The Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009 Australia.
Karlia
K
Meitha
School of Plant Biology, and The Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009 Australia, Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, Universitetsparken 4, 2100 Copenhagen, Denmark.
Dennis
D
Konnerup
School of Plant Biology, and The Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009 Australia.
Timothy D
TD
Colmer
School of Plant Biology, and The Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009 Australia.
John A
JA
Considine
School of Plant Biology, and The Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009 Australia, Centre for Plant Sciences, University of Leeds, Leeds, Yorkshire LS29JT, UK and.
Christine H
CH
Foyer
School of Plant Biology, and The Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009 Australia, Centre for Plant Sciences, University of Leeds, Leeds, Yorkshire LS29JT, UK and Department of Agriculture and Food Western Australia, South Perth, WA, 6151 Australia michael.considine@uwa.edu.au.
Michael J
MJ
Considine
D000693:Anaerobiosis; D018519:Meristem / Q000378:metabolism; D010100:Oxygen / Q000378:metabolism*; D057445:Plant Dormancy; D017382:Reactive Oxygen Species / Q000378:metabolism*; D027843:Vitis / Q000254:growth & development* / Q000378:metabolism
D017382:Reactive Oxygen Species; D010100:Oxygen
Bud burst; ROS; Vitis vinifera; development; ecodormancy; grapevine; hypoxia; meristem; oxygen partial pressure; quiescence; reactive oxygen species; respiration; superoxide