Melatonin improves rice salinity stress tolerance by NADPH oxidase‐dependent control of the plasma membrane K⁺ transporters and K⁺ homeostasis

Abstract

This study aimed to reveal the mechanistic basis of the melatonin-mediated amelioration of salinity stress in plants. Electrophysiological experiments revealed that melatonin decreased salt-induced K + efflux (a critical determinant of plant salt tolerance) in a dose-and time-dependent manner and reduced sensitivity of the plasma membrane K +-permeable channels to hydroxyl radicals. These beneficial effects of melatonin were abolished by NADPH oxidase blocker DPI. Transcriptome analyses revealed that melatonin induced 585 (448 up-and 137 down-regulated) and 59 (54 up-and 5 down-regulated) differentially expressed genes (DEGs) in the root tip and mature zone, respectively. The most noticeable changes in the root tip were melatonininduced increase in the expression of several DEGs encoding respiratory burst NADPH oxidases (OsRBOHA and OsRBOHF), calcineurin B-like/calcineurin B-like-interacting protein kinase (OsCBL/OsCIPK), and calcium-dependent protein kinase (OsCDPK) under salt stress. Melatonin also enhanced the expression of potassium transporter genes (OsAKT1, OsHAK1, and OsHAK5). Taken together, these results indicate that melatonin improves salt tolerance in rice by enabling K + retention in roots, and that the latter process is conferred by melatonin scavenging of hydroxyl radicals and a concurrent OsRBOHF-dependent ROS signalling required to activate stress-responsive genes and increase the expression of K + uptake transporters in the root tip.

Molecular hydrogen–induced salinity tolerance requires melatonin signalling inArabidopsis thaliana

“…Subsequent pharmacological evidence confirmed that sodium orthovanadate or amiloride significantly blocked both Na + effluxes and H + influxes in NaCl‐stressed CrHYD1 roots, and contrasting changes were found in K + effluxes (Figure 5). Similar to the previous reports (Liu et al, 2020; Sun et al, 2008; J. Zhang et al, 2016), above results indicated that MT‐dependent Na + extrusion (Figures 3a and 4a) in CrHYD1 transgenic lines was partly the result of an active Na + /H + antiport across the plasma membrane (Chen et al, 2007). Combined with the results in Figures 3 and 4, our findings provided evidence that endogenous H 2 regulated MT‐dependent positive ion transport, possibly explaining why CrHYD1 transgenic plants have greater tolerance to salt stress.…”

“…The data above were consistent with the results in Figure 3. Similar changes for ion fluxes in salt‐resistant plants were also reported (Liu et al, 2020; Sun et al, 2008; J. Zhang et al, 2016). Subsequent pharmacological evidence confirmed that sodium orthovanadate or amiloride significantly blocked both Na + effluxes and H + influxes in NaCl‐stressed CrHYD1 roots, and contrasting changes were found in K + effluxes (Figure 5).…”

“…Interestingly, the physiological roles of endogenous H 2 were impaired in atsnat / CrHYD1‐4 (Figure 3a–c), suggesting that MT might mediate endogenous H 2 –induced positive ion transport. Similar to the previous results obtained in Solanum lycopersicum L ., Arabidopsis and rice (Chen et al, 2017; Liu et al, 2020; Yan et al, 2019), we further confirmed that MT participated in the reestablishment of ion homeostasis in plants upon salinity stress.…”

“…Melatonin (MT) and hydrogen gas (H 2 ) have emerged as important signal molecules that play multitudinous roles in plant development and stress responses (Arnao & Hernandez‐Ruiz, 2015, 2019; C. Li et al, 2018; Liu et al, 2020; Wu et al, 2020; Yan et al, 2019; Z. Zhang et al, 2019; Y. Zhang et al, 2020). However, no reports have yet been made with respect to the relationship between MT and H 2 in response to an abiotic stress, such as salinity.…”

“…It remains to be fully understood how endogenous H 2 regulates the synthesis of MT. In response to salt stress, both H 2 and MT can be adopted in stress‐triggered signalling pathways (Chen et al, 2017; Liang et al, 2015; Liu et al, 2020; Xie et al, 2012; S. Xu et al, 2013), whereby other shared transduction components may exert positive modulating roles on alternative pathways. So, other possible downstream signalling of endogenous H 2 for increasing plant salinity tolerance should be explored.…”