Genome-wide association analysis locates FtAUR3 in Tartary buckwheat that contributes to enhance plant salt resistance

doi:10.1016/j.jia.2025.04.008

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Xiang Lu^1,2^*, Qian Zuo²^*, Md. Nurul Huda^2#, Yaliang Shi², Guangsheng Li², Xiangru Wang², Yawen Xiao², Muhammad Khurshid³, Tanzim Jahan², Namraj Dhami⁴, Dhurva Prasad Gauchan⁵, Md. Arfan Ali⁶, Jianping Cheng¹, Yu Meng⁷, Jingjun Ruan¹^#, Meiliang Zhou²^#

¹College of Agriculture, Guizhou University, Guiyang 550025, China

²Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing100081, China

³School of Biochemistry and Biotechnology, University of the Punjab, Lahore 54590, Pakista.

⁴School of Health and Allied Sciences, Faculty of Health Sciences, Pokhara University, Dhungepatan, Pokhara-30, Kaski 33700, Nepal

⁵Department of Biotechnology, School of Science, Kathmandu University, Dhulikhel 45200, Nepal.

⁶Department of Horticulture, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka-1207, Bangladesh

⁷Country College of Landscape Architecture and Tourism, Hebei Agricultural University, Baoding 071001, China

Highlights

● The method of GWAS with transcriptomic analysis enhances confidence in linking genetic loci to functional responses under stress.

● The results of FtAUR3 could bridge ROS management with energy production under stress.

● The identified SNP of FtAUR3 promoter can be useful for marker-assisted breeding.

Abstract
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摘要

荞麦（Fagopyrum tataricum）是一种未充分利用的孤儿作物，具有重要的营养和药用价值，且对逆境有较好的耐受性。然而，这种环保作物对盐胁迫敏感，盐胁迫会导致水分流失、气孔关闭，影响光合作用和代谢，降低荞麦的产量和质量。因此，了解荞麦的盐胁迫耐受机制至关重要。在本研究中，我们通过全基因组关联分析（GWAS）确定了在第2号染色体上包含35个候选基因的位点，这个位点与荞麦的盐耐受性显著相关。转录组分析表明，丝氨酸/苏氨酸蛋白激酶 Aurora-3（FtAUR3）家族基因在盐胁迫下上调表达。在 FtAUR3 启动子中单核苷酸的缺失会导致 FtAUR3 表达增加，从而增强荞麦对盐的耐受性。FtAUR3 在荞麦毛状根中的过表达导致了类黄酮的积累，包括芦丁和肉桂酸，并在盐胁迫下诱导了类黄酮生物合成基因（如PAL、C4H、F3H和F3’H）的表达。此外，过表达 FtAUR3 的拟南芥相较于野生型拟南芥增强了盐耐受基因（SOS1、AVP1等）的表达，增强了植物对盐胁迫的耐受性。同时，在盐胁迫下，FtAUR3 显著提高了 ROS 通路成分的水平，包括超氧化物歧化酶、过氧化氢酶和过氧化物酶，进而改善植物的盐耐受性。另外，我们证明了 FtAUR3 与 ROS 通路中的关键酶 FtGAPB 相互作用，提出了 FtAUR3 参与 ROS 信号的潜在机制。综合这些结果，证实了 FtAUR3 在荞麦耐盐胁迫中可能发挥重要的积极作用。

Abstract

Tartary buckwheat (Fagopyrum tataricum), an under-utilized pseudocereal, has important nutritional and pharmaceutical properties and is resistant to drought and nutrient deficiency. However, this environmentally friendly crop is sensitive to salt stress that can result in water loss, stomatal closure, affect photosynthesis and metabolism, and reduce yield and quality of Tartary buckwheat. Thus, it is important to understand the mechanism of salt stress tolerance in buckwheat. In this study, we identified a locus including 35 candidate genes on chromosome 2 that is significantly associated with salt tolerance of Tartary buckwheat by genome-wide association analysis (GWAS). Transcriptome analysis revealed that the serine/threonine-protein kinase Aurora-3 (FtAUR3) family gene was up-regulated in response to salt stress. The deletion of a single nucleotide in the FtAUR3 promoter leads to increased FtAUR3 expression and enhanced salt tolerance in Tartary buckwheat. Overexpression of FtAUR3 in buckwheat hairy roots leads to the accumulation of flavonoids, including rutin and cinnamic acid, as well as the induction of the expression of flavonoid biosynthesis genes, such as PAL, C4H, F3H and F3’H, under salt stress. In addition, it was shown that over-expression of FtAUR3 in Arabidopsis thaliana induced the expression of salt-resistant genes (SOS1, AVP1, etc.) and enhanced salt tolerance compared to wild type plants. Furthermore, under salt stress, FtAUR3 can significantly enhances the levels of reactive oxygen species pathway components, including superoxide dismutase, catalase, and peroxidase, thereby improving plant salt tolerance. Thus, we demonstrated that FtAUR3 interacts with the critical enzyme FtGAPB in the ROS pathway, suggesting a potential mechanism through which FtAUR3 contributes to ROS signaling. Taken together, these results demonstrated that FtAUR3 may play a critical positive role in Tartary buckwheat resistance against salt stress.

Keywords: Fagopyrum tataricum GWAS aurora-3 salt stress gairy roots Arabidopsis thaliana

Received: 20 January 2025 Online: 03 April 2025

Fund:

This research was supported by the Asian Cooperation Fund Project (102125241610090000029), the National Key R&D Program of China (2019YFD1001300 and 2019YFD1001305), the Natural Science Foundation of Hebei Province, China (C2023204097) and the National Science Foundation of China (31560578, Cheng JP, http://www.nsfc.gov.cn).

About author: #Correspondence E-mail: zhoumeiliang@caas.cn; Jingjun Ruan, E-mail: jjruan@gzu.edu.cn *Equal contributors

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Xiang Lu, Qian Zuo, Md. Nurul Huda, Yaliang Shi, Guangsheng Li, Xiangru Wang, Yawen Xiao, Muhammad Khurshid, Tanzim Jahan, Namraj Dhami, Dhurva Prasad Gauchan, Md. Arfan Ali, Jianping Cheng, Yu Meng, Jingjun Ruan, Meiliang Zhou. 2025. Genome-wide association analysis locates FtAUR3 in Tartary buckwheat that contributes to enhance plant salt resistance. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.04.008

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