Unveiling morphophysiological and metabolic adaptive strategies of the CAM epiphytic bromeliad Acanthostachys pitcairnioides to drought

• Published in: Plant physiology and biochemistry 2024-11, Vol.216, p.109076, Article 109076
• Main Authors: Batista, Ursula Caroline Salvaterra, Pereira, Everton Fernandes Teodoro, Hayashi, Adriana Hissae, Silva, Kleber Resende, Purgatto, Eduardo, Vieira, Evandro Alves, Gaspar, Marilia
• Format: Article
• Language: English
• Subjects: abscisic acid; Abscisic Acid - metabolism; Adaptation, Physiological; Anthocyanins; Bromeliaceae; Bromeliaceae - metabolism; Bromeliaceae - physiology; carbon; carotenoids; chlorenchyma; chlorophyll; Chlorophyll - metabolism; climate; Crassulacean acid metabolism; drought; Droughts; epiphytes; forests; irrigation; isotopes; Isotopic 13C signature; jasmonic acid; leaves; Metabolic profiling; metabolites; myo-inositol; Osmoregulation; Photochemical activity; photochemistry; photosynthesis; Photosynthesis - physiology; Plant Leaves - metabolism; proline; rehydration; salicylic acid; trehalose; turgor; Water - metabolism; water content; water storage; Water storing hydrenchyma; water stress
• ISSN: 0981-9428; 1873-2690; 1873-2690
• DOI: 10.1016/j.plaphy.2024.109076

Ongoing climate changes are expected to intensify drought periods in tropical regions, directly impacting epiphytic bromeliads that depend on intermittent water availability. This study aimed to elucidate if Acanthostachys pitcairnioides, an epiphytic bromeliad of Atlantic Forest, tolerates extended drought periods and the potential strategies involved in its tolerance and recovery capacity. We suppressed irrigation for 42 days, rehydrated plants for four days, and evaluated leaf water status, and photochemical, metabolic, and anatomical changes. During the initial 28 days of drought, translocation of water from hydrenchyma to chlorenchyma, higher chlorophyll content, and accumulation of abscisic and salicylic acid and antioxidants contributed to maintaining the cell turgor and functionality of photosynthetic apparatus. At 42 days, a significant reduction in leaf water content to 45.5% was accompanied by a 2.5-fold increase in non-photochemical quenching and enhanced levels of carotenoids, anthocyanins, osmoregulators (proline, myo-inositol, and trehalose), and phytohormones (abscisic acid and jasmonates). After rewatering, water storage in the hydrenchyma and almost all pigments, hormones, and metabolites were restored to pre-stress conditions. Leaf succulence, carbohydrate and organic acid accumulation, and carbon isotope data (δ13C−14.5‰) provide evidence of induction of CAM metabolism by water limitation in A. pitcairnioides. Our findings indicate the prevalence of water accumulation strategy during the first half of the drought stress. At the end of the drought period, the complete depletion of water from the hydrenchyma favored the osmotic adjustment. Considering this set of tolerance strategies and the rapid recovery after rehydration, A. pitcairnioides can successfully withstand environments with restricted water availability. [Display omitted] •The epiphytic bromeliad Acanthostachys pitcairnioides withstand 42 days of drought.•The translocation of water to chlorenchyma preserved the photosynthetic apparatus.•Increased content of carotenoids and anthocyanins avoided strong photoinhibition.•As drought intensifies, water preservation strategy shifts to osmotic adjustment.•Malate accumulation and δ13C close to −15‰ corroborate CAM metabolism.