Combined Metabolomic and Transcriptomic Analysis Reveals Allantoin Enhances Drought Tolerance in Rice

Abstract

Drought is a misfortune for agriculture and human beings. The annual crop yield reduction caused by drought exceeds the sum of all pathogens. As one of the gatekeepers of China’s “granary”, rice is the most important to reveal the key drought tolerance factors in rice. Rice seedlings of Nipponbare (Oryza sativa L. ssp. Japonica) were subjected to simulated drought stress, and their root systems were analyzed for the non-targeted metabolome and strand-specific transcriptome. We found that both DEGs and metabolites were enriched in purine metabolism, and allantoin accumulated significantly in roots under drought stress. However, few studies on drought tolerance of exogenous allantoin in rice have been reported. We aimed to further determine whether allantoin can improve the drought tolerance of rice. Under the treatment of exogenous allantoin at different concentrations, the drought resistant metabolites of plants accumulated significantly, including proline and soluble sugar, and reactive oxygen species (ROS) decreased and reached a significant level in 100 μmol L−1. To this end, a follow-up study was identified in 100 μmol L−1 exogenous allantoin and found that exogenous allantoin improved the drought resistance of rice. At the gene level, under allantoin drought treatment, we found that genes of scavenge reactive oxygen species were significantly expressed, including peroxidase (POD), catalase (CATA), ascorbate peroxidase 8 (APX8) and respiratory burst oxidase homolog protein F (RbohF). This indicates that plants treated by allantoin have better ability to scavenge reactive oxygen species to resist drought. Alternative splicing analysis revealed a total of 427 differentially expressed alternative splicing events across 320 genes. The analysis of splicing factors showed that gene alternative splicing could be divided into many different subgroups and play a regulatory role in many aspects. Through further analysis, we restated the key genes and enzymes in the allantoin synthesis and catabolism pathway, and found that the expression of synthetase and hydrolase showed a downward trend. The pathway of uric acid to allantoin is completed by uric acid oxidase (UOX). To find out the key transcription factors that regulate the expression of this gene, we identified two highly related transcription factors OsERF059 and ONAC007 through correlation analysis. They may be the key for allantoin to enhance the drought resistance of rice.

Exogenous Allantoin Confers Rapeseed (Brassica campestris) Tolerance to Simulated Drought by Improving Antioxidant Metabolism and Physiology

“…In our experiment, the H 2 O 2 content as well as lipid peroxidation (MDA levels) and EL of the rapeseed plants were notably increased when exposed to drought. Drought also showed an upregulated ROS generation in rice, previously recorded by Lu et al [65]. However, exogenous allantoin mitigated H 2 O 2 , MDA, and EL of the drought-stressed plants in our experiment.…”

“…Allantoin application upregulated the ABA biosynthesis gene, OsUGT85E1, which accelerates the accumulation of ABA, induces stomatal closure, and enhances the ROS scavenging capacity of rice under drought [ 64 ]. Allantoin also plays a key role in synthesizing jasmonic acid under drought through the ABA pathway and improved resistance to drought, as reported by Lu et al [ 65 ]. Potassium ions regulate stomatal opening and closing to reduce water losses through stomata under drought [ 66 ], and their accumulation was lowered upon allantoin treatment in our experiment.…”

“…Previous studies also demonstrated that the accumulation of allantoin and allantoate accelerates the ureide metabolic pathway and mitigates the ability of ROS to confer various stresses [ 26 , 63 , 73 ]. Lu et al [ 65 ] demonstrated that drought escalated ROS production in rice, but the ROS were decreased when the seeds were grown in allantoin-incorporated growing media. The RNAi xanthine dehydrogenase mutants were reported to be more susceptible to drought [ 74 ].…”

When drought meets heat – a plant omics perspective

“…To safeguard cells from stress-induced damage, plants adapt by reprogramming their metabolic pathways. While there are several metabolome datasets under individual drought and heat stress ( Ye et al., 2016 ; Sun et al., 2019 ; Abdelrahman et al., 2020 ; Lecourieux et al., 2020 ; Guo et al., 2021 ; Lu et al., 2022 ; López et al., 2023 ; Xie et al., 2023 ), there are only a few studies with respect to combined stress ( Zinta et al., 2018 ; Alhaithloul et al., 2019 ; Lawas et al., 2019 ; Qaseem et al., 2019 ; Xie et al., 2020 ; Yousaf et al., 2022 ; Ru et al., 2023 ). Under combined stress, the processes of carbohydrate metabolism, amino acid metabolism and organic acid are differentially affected compared with a non-stress condition ( Zinta et al., 2018 ; Lawas et al., 2019 ).…”

Crystal Structure of Allantoinase from Escherichia coli BL21: A Molecular Insight into a Role of the Active Site Loops in Catalysis

“…Allantoin in plants participates in many positively signaling regulations and is also a signaling chemical that conveys information on local conditions in plant–plant interactions [ 6 ]. For example, allantoin enhances drought tolerance in rice [ 7 ]. In addition, allantoin also positively affects salt tolerance by increasing the reactive oxygen species scavenging capacity and maintaining sodium and potassium homeostasis [ 8 ].…”