β-cyclocitric acid: a new apocarotenoid eliciting drought tolerance in plants

Abstract

15This article contains supporting information online. 16 2 -Cyclocitral (-CC) is a volatile compound deriving from 1 O2 oxidation of -carotene in plant 17 leaves. -CC elicits a retrograde signaling, modulating 1 O2-responsive genes and enhancing 18 tolerance to photooxidative stress. Here, we show that -CC is largely converted into -19 cyclocitric acid (-CCA) in leaves and that this metabolite is a signal involved in stress 20 tolerance. Treatment of Arabidopsis plants with -CCA markedly enhanced plant tolerance 21 to drought by a mechanism different from known responses such as stomatal closure, 22 changes in osmotic potential and jasmonate signaling. Furthermore, we show that the 23 response to -CCA does not fully overlap with the -CC-dependent signaling, indicating that 24 -CCA induces only a branch of the -CC signaling pathway. In addition, the protective effect 25 of -CCA is a conserved mechanism, being observed in a variety of plant species. This study 26 provides a new bioactive agent with promising agronomic applications for protecting plants 27 against drought. 28 29 30 31 32 33 34 35 36 37 38 39 40 3Oxidation of the carotenoid -carotene by reactive oxygen species (ROS), especially singlet 41 oxygen ( 1 O2), produces various derivatives (apocarotenoids) including -cyclocitral (-CC) 1,2 . 42 This phenomenon was shown to take place in plant leaves and enhanced under stress 43 conditions 1,2 . In fact, when plants are exposed to environmental constraints (i.e. drought, cold 44 or pathogens), which inhibit the photosynthetic activity, light energy can be absorbed in 45 excess to what can be used by the photosynthetic processes, hence favoring transfer of 46 electrons or excitation to oxygen and leading to ROS formation 3,4 . Singlet oxygen is produced 47 from triplet-excited chlorophylls, mainly in the PSII reaction centers 5-8 . In fact, the PSII centers 48 bind several -carotene molecules that can scavenge 1 O2 molecules generated therein 5,9 . 1 O2 49 quenching by carotenoids proceeds by a physical mechanism that leads to thermal energy 50 dissipation 10 and also through a chemical quenching mechanism involving direct oxidation of 51 the carotenoid molecule by 1 O2 2,5,11 . Thus, as a major site of 1 O2 production, PSII is also a major 52 generator of oxidized -carotene metabolites such as -CC. 53

Sensing β‐carotene oxidation in photosystem II to master plant stress tolerance

“…This oxidation occurs spontaneously in water (Tomita et al ., ). We recently demonstrated that this molecule exists in Arabidopsis at higher concentrations than β‐CC (D'Alessandro et al ., ). Therefore, we can hypothesize several fates for β‐CC, depending on which side of the thylakoid membrane it is released from PSII.…”

“…Arabidopsis plants pre‐treated with volatile β‐CC or dhA exhibited lower lipid peroxidation and lower PSII photoinhibition after high light stress compared to untreated plants (Ramel et al ., ; Shumbe et al ., , ). β‐CC and β‐CCA were also found to enhance drought tolerance of Arabidopsis plants (D'Alessandro et al ., ). Both stresses are known to modulate PAP accumulation (Estavillo et al ., ).…”

“…By inducing SCL14‐dependent xenobiotic response, β‐CC prepares the cell for the accumulation of lipid peroxides occurring under excess light or drought stress by increasing detoxification of toxic RCS (D'Alessandro et al ., ). Similar to β‐CC treatment, the overexpressor lines of SCL14 were more tolerant both to excess light and to drought stress (D'Alessandro et al ., ,). Drought and oxidative tolerance was also confirmed in rice by the overexpressor lines of the SCL14 homologue OsGRAS23 (Xu et al ., ).…”