Department of Botany, Ecology and Plant Physiology, University of La Laguna (ULL), Tenerife 38200, Spain.
Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Barrio Sarriena s/n, 48940 Leioa, Spain.
J Exp Bot. 2021 Apr 2;72(8):3168-3184. doi: 10.1093/jxb/erab071.
While most ferns avoid freezing as they have a tropical distribution or shed their fronds, wintergreen species in temperate and boreoalpine ecosystems have to deal with sub-zero temperatures. Increasing evidence has revealed overlapping mechanisms of desiccation and freezing tolerance in angiosperms, but the physiological mechanisms behind freezing tolerance in ferns are far from clear. We evaluated photochemical and hydraulic parameters in five wintergreen fern species differing in their ability to tolerate desiccation. We assessed frond freezing tolerance, ice nucleation temperature and propagation pattern, and xylem anatomical traits. Dynamics of photochemical performance and xanthophyll cycle were evaluated during freeze-thaw events under controlled conditions and, in selected species, in the field. Only desiccation-tolerant species, which possessed a greater fraction of narrow tracheids (<18 μm) than sensitive species, tolerated freezing. Frond freezing occurred in the field at -3.4 ± 0.9 °C (SD) irrespective of freezing tolerance, freezable water content, or tracheid properties. Even in complete darkness, maximal photochemical efficiency of photosystem II was down-regulated concomitantly with zeaxanthin accumulation in response to freezing. This was reversible upon re-warming only in tolerant species. Our results suggest that adaptation for freezing tolerance is associated with desiccation tolerance through complementary xylem properties (which may prevent risk of irreversible cavitation) and effective photoprotection mechanisms. The latter includes de-epoxidation of xanthophylls in darkness, a process evidenced for the first time directly in the field.
虽然大多数蕨类植物因具有热带分布或脱落叶片而避免冻结，但温带和北方高山生态系统中的冬青木物种必须应对零度以下的温度。越来越多的证据表明，被子植物的脱水和抗冻机制存在重叠，但蕨类植物抗冻性背后的生理机制还远不清楚。我们评估了 5 种冬青木物种的光化学和水力参数，这些物种在耐受脱水的能力上存在差异。我们评估了叶片的抗冻性、冰核形成温度和传播模式，以及木质部解剖特征。在受控条件下和在选定的物种中，评估了光化学性能和叶黄素循环在冻融事件中的动态。只有具有比敏感物种更大比例的窄导管（<18 μm）的耐脱水物种才能耐受冻结。叶片在野外的冻结温度为-3.4 ± 0.9 °C（SD），与抗冻性、可冻结水含量或导管特性无关。即使在完全黑暗中，光合作用系统 II 的最大光化学效率也会与叶黄素积累同时下调，以响应冻结。只有在耐受物种中，这种下调才会在重新升温时恢复。我们的结果表明，抗冻性的适应与通过互补的木质部特性（这可能防止不可逆空化的风险）和有效的光保护机制与脱水耐受性相关。后一种机制包括叶黄素在黑暗中的去环氧化，这是首次在野外直接证明的过程。
