The Apocarotenoid β-Cyclocitric Acid Elicits Drought Tolerance in Plants

Abstract

Summary β-Cyclocitral (β-CC) is a volatile compound deriving from 1 O 2 oxidation of β-carotene in plant leaves. β-CC elicits a retrograde signal, modulating 1 O 2 -responsive genes and enhancing tolerance to photooxidative stress. Here, we show that β-CC is converted into water-soluble β-cyclocitric acid (β-CCA) in leaves. This metabolite is a signal that enhances plant tolerance to drought by a mechanism different from known responses such as stomatal closure, osmotic potential adjustment, and jasmonate signaling. This action of β-CCA is a conserved mechanism, being observed in various plant species, and it does not fully overlap with the β-CC-dependent signaling, indicating that β-CCA induces only a branch of β-CC signaling. Overexpressing SCARECROW-LIKE14 (SCL14, a regulator of xenobiotic detoxification) increased drought tolerance and potentiated the protective effect of β-CCA, showing the involvement of the SCL14-dependent detoxification in the phenomenon. β-CCA is a bioactive apocarotenoid that could potentially be used to protect crop plants against drought.

Effect of Drought on the Methylerythritol 4-Phosphate (MEP) Pathway in the Isoprene Emitting Conifer Picea glauca

“…For example, the decline in the carotenoid violaxanthin is associated with the activation of the xanthophyll cycle. The increase in β-cyclocitral under severe drought may also help enhance tolerance toward oxidative stress after its conversion to β-cyclocitric acid ( D’Alessandro et al, 2019 ). Although we did not measure tocopherols, these isoprenoid antioxidants could also reduce oxidative stress.…”

Oxygen and ROS in Photosynthesis

“…The lifetime of 1 O 2 in plant cells has not been measured, but is generally assumed to be too short (for review, see [23]; Section 2.1.4) to enable diffusion out of chloroplasts and, consequently, 1 O 2 itself is unlikely to function as a messenger molecule. Instead, the accumulation of β-CC (a reaction product of β-carotene and 1 O 2 ) has been shown to induce gene expression, leading to stress (e.g., high light) acclimation [391,409,410]. In theory, β-CC could directly travel to the nucleus and activate 1 O 2 responsive genes (for discussion, see [411]), however, direct evidence is lacking.…”

“…Methylene Blue Sensitivity 1 protein might participate in transferring the signal from cytosol to the nucleus [412,413]. In addition, β-CC can be converted to water-soluble β-cyclocitric acid, which also could function as a signaling molecule [410]. Other oxidation products of 1 O 2 might have signaling functions, too [346,414].…”

Apocarotenoids Involved in Plant Development and Stress Response

“…β-Cyclocitral is an example for a carotenoid cleavage product that can be formed following both scenarios (Ramel et al, 2012b; Rodrigo et al, 2013). The formation of this β-carotene–derived volatile in photosynthetic tissues is triggered by a singlet oxygen 1 O 2 attack, which takes place in the photosystem II, particularly under high light stress (D’Alessandro et al, 2019), while in citrus fruits, it is catalyzed by a CCD (CCD4b) that cleaves β-carotene, β-cryptoxanthin, and zeaxanthin (Rodrigo et al, 2013). Although some CCDs show a quite relaxed substrate and site (double bond) specificity (Ilg et al, 2014), cleavage reactions catalyzed by these enzymes generally take place at certain double bond(s) in defined carotenoid/apocarotenoid substrate(s) (Walter and Strack, 2011; McQuinn et al, 2015).…”