Metabolic profiling of epidermal and mesophyll tissues under water-deficit stress in Opuntia ficus-indica reveals stress-adaptive metabolic responses
Jesse A. Mayer A B , Bernard W. M. Wone C , Danny C. Alexander D , Lining Guo D , John A. Ryals D and John C. Cushman
A E
+ Author Affiliations
- Author Affiliations
A Department of Biochemistry and Molecular Biology, University of Nevada, Reno, NV 89557, USA.
B Present address: Thermo Fisher Scientific, Carlsbad, CA 92008, USA.
C Department of Biology, University of South Dakota, SD 57069, USA.
D Metabolon Inc., 800 Capitola Drive, Suite 1, Durham, NC 27713, USA.
E Corresponding author. Email: jcushman@unr.edu
Functional Plant Biology 48(7) 717-731 https://doi.org/10.1071/FP20332
Submitted: 24 October 2020 Accepted: 20 February 2021 Published: 26 April 2021
Abstract
Cactus pear (Opuntia ficus-indica) is a high productivity species within the Cactaceae grown in many semiarid parts of the world for food, fodder, forage, and biofuels. O. ficus-indica utilises obligate crassulacean acid metabolism (CAM), an adaptation that greatly improves water-use efficiency (WUE) and reduces crop water usage. To better understand CAM-related metabolites and water-deficit stress responses of O. ficus-indica, comparative metabolic profiling was performed on mesophyll and epidermal tissues collected from well-watered and water-deficit stressed cladodes at 50% relative water content (RWC). Tissues were collected over a 24-h period to identify metabolite levels throughout the diel cycle and analysed using a combination of acidic/basic ultra-high-performance liquid chromatography/tandem mass spectrometry (UHPLC/MS/MS) and gas chromatography/mass spectrometry (GC/MS) platforms. A total of 382 metabolites, including 210 (55%) named and 172 (45%) unnamed compounds, were characterised across both tissues. Most tricarboxylic acid (TCA) cycle and glycolysis intermediates were depleted in plants undergoing water-deficit stress indicative of CAM idling or post-idling, while the raffinose family oligosaccharides (RFO) accumulated in both mesophyll and epidermal tissues as osmoprotectants. Levels of reduced glutathione and other metabolites of the ascorbate cycle as well as oxylipins, stress hormones such as traumatic acid, and nucleotide degradation products were increased under water-deficit stress conditions. Notably, tryptophan accumulation, an atypical response, was significantly (24-fold) higher during all time points in water-deficit stressed mesophyll tissue compared with well-watered controls. Many of the metabolite increases were indicative of a highly oxidising environment under water-deficit stress. A total of 34 unnamed metabolites also accumulated in response to water-deficit stress indicating that such compounds might play important roles in water-deficit stress tolerance.
Keywords: crassulacean acid metabolism, CAM, metabolic profiling, cactus pear, Opuntia ficus-indica, water-deficit stress, epidermis, mesophyll, tryptophan.
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