Please cite this paper as:

Back, K., Tan, D.-X. and Reiter, R.J. 2021. Strategies to generate melatonin-enriched transgenic rice to respond to the adverse effects on rice production potentially caused by global warming. Melatonin Research. 4, 4 (Dec. 2021), 501-506. DOI:https://doi.org/https://doi.org/10.32794/mr112500108.


Commentary

 

Strategies to generate melatonin-enriched transgenic rice to respond to the adverse effects on rice production potentially caused by global warming

Kyoungwhan Back1*, Dun-Xian Tan2, Russel J. Reiter2

 1Department of Biotechnology, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 61186, Republic of Korea

2Department of Cell Systems and Anatomy, University of Texas Health Science Center, San Antonio, Texas, USA

*Correspondence: kback@chonnam.ac.kr, Tel: +82625302165

Running title: Stress tolerance of melatonin-enriched rice and global warming

Received: October 20, 2021; Accepted: November 23, 2021

 

ABSTRACT

     Global warming is predicted to reduce the yield of rice, which feeds more than half of the world’s population. A rise in temperature will inevitably hamper rice production by causing drought and flooding. Melatonin has the capacity to ameliorate such adverse effects. Here, we propose multiple genetic means of producing melatonin-enriched, high-yield rice variants to adapt upcoming global warming.

Key words: melatonin, global warming, arsenic, high temperature, drought

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   Global warming has a negative effect on agricultural production (1). In 2014, the International Panel on Climate Change (IPCC) initially predicted a 1.5–2.0°Cincrease in global temperature by the end of this century, but in 2017 this was reevaluatedto a 5°Cincrease (2). Rice yields are more vulnerable to the nighttime temperature changes than that in daytime (3). Ceccarelli et al. (4) have predicted that a temperature increase will reduce rice production up to 41% by the end of the 21st century and reduce maize production up to 50% by 2080. This prediction is linked to a report that yields of rice grain may decline by 10% for each 1°Crise above growing-season’s normal temperature (5). Temperatures higher than the optimum decrease photosynthesis (6) and cause drought; thereby, reducing rice yield as well (7). A high temperature during the flowering and grain-ripening stages significantly decreases seed fertility and grain-filling rate, as well as rice yield (8). Worldwide, rice production is hampered by high temperature, drought, floods, pathogens, salt stress, and arsenic stress (9). Clearly, a means of overcoming the adverse effects of global warming on rice production is needed.

   Globally, annual rice production is around 782 million tons and this grain contributes to the food supply of more than half of the world’s population (10). To maintain current rice production levels, efforts have focused on improving cultivation practices and breeding new rice variants that are more resistant to stresses caused by global warming.

 Melatonin is an indoleamine with diverse physiological roles in animals and plants (11). Since its discovery in plants in 1995 (12, 13), approximately 800 papers on melatonin in plants have been published (14). Melatonin as a potent antioxidant can quench up to 10 molecules of reactive oxygen species (ROS) and lacks prooxidant activity (15, 16). In fact, melatonin protects plants from chemical stressors that generate ROS (17). These stressors include cadmium, lead, aluminum, copper, vanadium, methyl viologen, and herbicides. Exogenous application of melatonin or an increase in endogenous melatonin in transgenic plants enhances tolerance of plants to these stressors (18). With regard to arsenic accumulation in rice grain, melatonin confers arsenic stress tolerance by enhancing antioxidant activity in soybean (19) and tea plants and decreases the arsenic content of tea (20), suggesting that it blocks arsenic translocation from roots to aboveground tissues, as it also does for cadmium (21, 22). Melatonin also enhances tolerance to abiotic stresses that cause oxidative damage by directly scavenging toxic radicals and by elevating the activities of antioxidant enzymes via induction of the expression of signaling and defense genes (23, 24). These abiotic stresses include drought, salinity, heat, cold, intense light, alkalinity, and acidity (25). Biotic stresses including bacteria, fungi, and viruses have also been attenuated by exogenous melatonin application and in melatonin-enriched transgenic plants (26, 27).

   To generate melatonin-enriched transgenic rice plants, it needs to understand melatonin biosynthetic and catabolic pathways in plants. Melatonin synthesis begins with the conversion of tryptophan into tryptamine by tryptophan decarboxylase (TDC). In the rice genome, there are at least three TDC genes, of which TDC1 (AK069031) and TDC3 (Os08g0140500) have 87% amino acid homology, compared to 47% and 48% homology to TDC2 (AK103253), respectively (28). The optimum TDC gene for melatonin production is TDC3. Tryptamine 5-hydroxylase (T5H) in rice catalyzes the conversion of tryptamine to serotonin. Therefore, ectopic overexpression of T5H in rice could increase melatonin levels (29). Serotonin N-acetyltransferase (SNAT) is responsible for N-acetylserotonin synthesis from serotonin. Two SNAT isogenes (SNAT1 and SNAT2) have been functionally characterized (24), but there are others in the rice genome (30). Ectopic overexpression of SNAT1 and SNAT2 increases melatonin in rice but the role of the rice ortholog of apple SNAT3 (AK109295) is unknown. Finally, N-acetylserotonin O-methyltransferase (ASMT) converts N-acetylserotonin into melatonin. A diverse array of O-methyltransferase enzymes shows ASMT activity, including caffeic acid O-methyltransferase (COMT) (24). The melatonin synthetic pathway is illustrated in Figure 1.

   In an earlier study on rice, overexpression of three ASMT genes (ASMT1, ASMT2, ASMT3) increased melatonin content, albeit only slightly (31). By contrast, COMT-overexpressing transgenic rice plants produce more melatonin than ASMT1–3-overexpressing plants (32). The putative rice ASMT4 (XM_015782901), which is orthologous to apple MzASMT9, localizes to chloroplasts (33) and has potential to enhance melatonin production (24). Overexpression of a novel ASMT5 gene (AK068864) in rice increases melatonin production twofold (34).

   Several melatonin catabolic genes have been cloned, including melatonin 2-hydroxylase (M2H), melatonin 3-hydroxylase (M3H), and N-acetylserotonin deacetylase (ASDAC) (24). M2H catalyzes conversion of melatonin into 2-hydroxymmelatonin whereas M3H converts melatonin into cyclic 3-hydroxymelatonin. Interestingly, ASDAC catalyzes the conversion of N-acetylserotonin into serotonin (35). These genes can be manipulated by genome-editing technologies, such as the CRISPR-Cas system. ASDAC (AK072557) exists as a single copy in the rice genome, enabling the generation of ASDAC-knockout mutant rice by CRISPR-Cas. The rice ASDAC mutant has blocked the reverse way of melatonin synthesis from N-acetylserotonin to serotonin, leading to melatonin accumulation. Rice possesses at least four copies of M2H (36) and at least three copies of M3H (37) with different Vmax values. There require stepwise mutant generations from quadruple to triple in M3H (m3h1/2/3/4) and M2H (m2h1/2/3) mutation to generate mutant rice with elevated melatonin synthesis. Melatonin production also can be increased using melatonin biosynthetic genes from other plants or animal species as well as by modifying melatonin biosynthesis, such as by overexpressing COMT in chloroplasts (38) (Figure 1).

Figure 1-1.jpg



Fig. 1. Melatonin synthetic pathway and the enzymes which can be genetically manipulated to increase endogenous melatonin levels in rice.

     The common abiotic stresses in rice plants including drought and flooding associated with global warming are highlighted in bold letters. Genes involved in melatonin biosynthesis and catabolism which can be used to increase the endogenous melatonin content of rice are marked as blue color. The bars indicate the block effect. The genetic modifications can be achieved by constitutively overexpressing melatonin biosynthetic genes under the control of a strong constitutive promoter, such as that of maize ubiquitin. Genes involved in melatonin catabolism (M2H, M3H) and the reverse pathway (ASDAC) can be knocked out by genome editing using the CRISPR-Cas system to increase the melatonin levels. TDC, tryptophan decarboxylase; T5H, tryptamine 5-hydroxylase; SNAT, serotonin N-acetyltransferase; ASMT, N-acetylserotonin O-methyltransferase; COMT, caffeic acid O-methyltransferase; ASDAC, N-acetylserotonin deacetylase; M2H, melatonin 2-hydroxylase; M3H, melatonin 3-hydroxylase. 

   In sumary, melatonin-enriched rice plants can be produced by overexpressing melatonin synthetic genes or knocking out melatonin catabolic genes. The most effective genes must be determined empirically to select transgenic rice plants with high melatonin contents but no growth inhibition or yield reduction. Melatonin-enriched rice not only has high yield but most importantly, be tolerant to climate change, such as global warming.

 

ACKNOWLEDGEMENTS

 This research was supported by a grant from the BioGreen 21-linked Innovative Agricultural Research and Development Program (Project No. PJ015703012021) funded by the Rural Development Administration, Republic of Korea. Yushin Back assisted with the preparation of figure 1.

 

AUTHORSHIP

 All authors contributed to the conceptualization, writing and editing of this article.


CONFLICT INTEREST

 The authors report no conflict of interest.

 

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