Exogenous Melatonin Improves Waterlogging Tolerance in Wheat through Promoting Antioxidant Enzymatic Activity and Carbon Assimilation

Abstract

In a pot experiment, we explored the regulatory pathways through which melatonin (MT) protects wheat growth and grain yield loss from waterlogging injury. Two wheat cultivars, Yangmai 18 and Yannong 19, were exposed to seven days of soil waterlogging at flowering. Melatonin (100 μmol·L−1) was sprayed before and after waterlogging to explore its regulation on root growth, photosynthetic characteristics, dry matter accumulation, and grain yield. Soil waterlogging intensified malondialdehyde (MDA) and O2− production rates in wheat tissues, impairing leaf photosynthesis, biomass accumulation, and final grain yield formation. In this study, the roots waterlogged at 7 days after anthesis (DAA) accumulated 20.9%, 76.2%, 17.6%, 28.5%, and 5.6% higher MDA content, O2− production rate, pyruvate decarboxylase (PDC), lactate dehydrogenase (LDH), and alcohol dehydrogenase (ADH) activities, respectively, in Yangmai 18, and 25.7%, 74.8%, 35.8%, 70.8%, and 30.7% higher in Yannong 19, respectively, compared with their respective non-waterlogged controls. Further, Yangmai 18 achieved a maximum net photosynthetic rate (Pn) reduction of 22.1% at 7 DAA, while the maximum Pn reduction of Yannong 19 was 27.4% at 14 DAA, respectively, compared with their respective non-waterlogged plants. Thus, waterlogging decreased total dry matter accumulation, 1000-grain weight (TGW), and total grain yield by 14.0%, 13.8%, and 16.2%, respectively, in Yangmai 18, and 16.0%, 8.1%, and 25.1%, respectively, in Yannong 19. Our study also suggests that exogenously applied melatonin can protect wheat root tissues from waterlogging-induced oxidative injury by upregulating antioxidant enzymes and sustaining leaf photosynthesis. The plants treated with melatonin showed better water status and less oxidative damage, which was conducive to maintaining a higher photosynthetic capacity, thereby improving the waterlogging tolerance of wheat. For example, compared with waterlogged plants, melatonin treatments significantly reduced MDA content, O2− production rate, PDC, LDH, and ADH activities by 7.7%, 25.4%, 2.6%, 32.1%, and 3.2%, respectively, in Yangmai 18, and 6.7%, 17.9%, 4.1%, 22.0%, and 15.3%, respectively, in Yannong 19. MT treatments significantly increased total dry matter accumulation, TGW, and yield by 5.9%, 8.7%, and 14.9%, respectively, in Yangmai 18, and 3.2%, 7.3%, and 26.0%, respectively, in Yannong 19.

Elucidating the modulatory effect of melatonin on enzyme activity and oxidative stress in wheat: a global meta‐analysis

“…These results highlight the importance of application methods in improving melatonin's advantageous effect on plant performance. The response to melatonin application varied among various wheat varieties (Dongxiao et al 2017, Ma et al 2022, Zhang et al 2022a). The current meta‐analysis showed that melatonin application on Lasani‐2008 and Giza168 wheat varieties resulted in higher enzymatic activities, whereas in Ujala‐216, these activities were significantly reduced.…”

“…Abiotic stresses are the major agricultural limitation that limits the crop growth and productivity of many crops worldwide. A previous study demonstrated that melatonin application significantly improved total dry matter accumulation and wheat yield by 5.9 and 14.9% in Yangmai 18, and 3.2 and 26.0% in Yannong 19, respectively (Ma et al 2022). Dongxiao et al (2017) reported that the effect of melatonin on drought resistance seedlings was diverse on wheat cultivars with different drought sensitivity, and melatonin was also involved in complex mechanisms involved in physiological regulation to retain water status.…”

Melatonin as a key regulator in seed germination under abiotic stress

“…Under anoxic conditions, rice mutants with the loss of functions of two enzymes involved in MEL biosynthesis (acetylserotonin methyl transferase [ASMT] and SNAT) showed retarded coleoptile and seedling growth, but the growth was recovered by the exogenous MEL application 145 . MEL regulates seedling growth under WL by mediating several other physiological processes including carbon assimilation, osmoregulation balance, and activating ROS scavenging system under anaerobic stress 146–148 . In general, MEL reprograms the biosynthesis and metabolism of ethylene (ET) and polyamines to improve WL tolerance 149–151 .…”

Photosynthetic adaptation mechanisms of waterlogged wheat (Triticum aestivum) at flowering under exogenous nitric oxide donor application

“…The pot and field experiments were conducted over two consecutive growing seasons, 2021-2022 and 2022-2023, at period was from the 3rd to the 10th day of April, while in cultivar YM15, it was from the 5th to the 12th day of April (Picture 1). The duration of the waterlogging period was determined based on previous findings where it was observed that the vigorous growth of all tested cultivars was significantly reduced after seven days of waterlogging in a field experiment (Ma et al, 2022a). Meanwhile, 150 μmol L À1 of sodium nitroprusside was sprayed on the 2nd, 4th, and 6th day during waterlogging in the WLsnp treatment in both cultivars.…”

“…The existing literature have extensively summarized the potential mechanisms that contribute to this phenomenon, including physical change in soil (i.e., soil compaction, oxygen depletion, CO 2 accumulation, and low diffusion coefficient for gases), chemical changes in soil (i.e., ion toxicity, secondary metabolite toxicity, low redox potential, and declined soil pH ), biological changes in soil (i.e., low mineralization rate, low aerobic microbial activity, and low immobilization rate) and low growth rate and poor metabolic capability of all organs in plants (Hossain and Uddin, 2011; Arduini et al, 2016; Herzog et al, 2016; Manik et al, 2019; Kaur et al, 2020; de S. Nóia Júnior et al, 2023). From the perspective of plant growth and metabolic processes, the primary impact of waterlogging on wheat plants is the insufficient supply of assimilates due to reduced photosynthetic production capacity during waterlogging (Cotrozzi et al, 2021; Ma et al, 2022a; Olorunwa et al, 2022; Li et al, 2023; Liu et al, 2023).…”