Liu Hai-Shuang, Liu Qin, Hepworth Shelley R, Li Pei-Qin, Huang Jie, Zhang Rui-Xin, Ma Cui-Min, Gao Tian-Ge, Ma Hong-Ping, Ke Jin, Bao Ai-Ke, Yin Hong-Ju, Flowers Timothy J, Luan Sheng, Ma Qing, Wang Suo-Min
State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, China.
Department of Biology, Institute of Biochemistry, Carleton University, Ottawa, Ontario, Canada.
Plant Biotechnol J. 2025 Sep;23(9):3497-3509. doi: 10.1111/pbi.70163. Epub 2025 Jun 4.
Uncovering the mechanisms underlying stress-resistant traits in xerophytes thriving in harsh environments can aid the genetic improvement of crops. The xerophyte Zygophyllum xanthoxylum features high Na accumulation in leaves, mediated by the vacuolar antiporter ZxNHX1. Co-expression of ZxNHX1 and vacuolar H-PPase gene ZxVP1-1 has been demonstrated to enhance the stress resistance and biomass of alfalfa. However, it remains unknown if ZxNHX1 outperforms its homologues from the Na-excluding and stress-sensitive glycophytes such as Arabidopsis in enhancing plant stress resistance and yield. Here, we found that expression of ZxNHX1 conferred superior growth under salt stress in alfalfa, compared to the Arabidopsis homologue AtNHX1. When expressed in yeast, ZxNHX1 displays stronger Na/H but weaker K/H exchange activity than AtNHX1. Under both K sufficient and deficient conditions, an Arabidopsis atnhx1-1 mutant expressing ZxNHX1 accumulated higher Na and lower K concentrations, with more Na being sequestered into vacuoles and a larger proportion of K retained in the cytosol. This optimized cellular ion distribution ensures energy-conserving osmotic adjustment, leading to stronger stress resistance and higher biomass than plants expressing AtNHX1. Moreover, ZxNHX1 governed the root uptake and root-to-leaf transport of Na at the whole-plant level, whereas AtNHX1 acted mainly in K transport processes. We also identified a polar residue Thr265 in a membrane-spanning region of ZxNHX1 that influences its Na and K selectivity. These findings reveal a new energy-conserving, Na-based osmotic adjustment mechanism that can enhance crop stress resistance without sacrificing yield, providing an effective way for utilizing saline soils to expand crop production into marginal lands.
揭示在恶劣环境中茁壮成长的旱生植物抗逆性状的潜在机制，有助于作物的遗传改良。旱生植物霸王具有较高的叶片钠积累量，这由液泡反向转运蛋白ZxNHX1介导。ZxNHX1与液泡H⁺-PPase基因ZxVP1-1的共表达已被证明可增强苜蓿的抗逆性和生物量。然而，ZxNHX1在增强植物抗逆性和产量方面是否优于来自非钠积累和胁迫敏感的甜土植物（如拟南芥）的同源物，仍不清楚。在这里，我们发现与拟南芥同源物AtNHX1相比，ZxNHX1的表达使苜蓿在盐胁迫下具有更好的生长表现。当在酵母中表达时，ZxNHX1比AtNHX1表现出更强的Na⁺/H⁺交换活性，但K⁺/H⁺交换活性较弱。在钾充足和缺乏的条件下，表达ZxNHX1的拟南芥atnhx1-1突变体积累了更高的钠浓度和更低的钾浓度，更多的钠被隔离到液泡中，更大比例的钾保留在细胞质中。这种优化的细胞离子分布确保了节能的渗透调节，导致比表达AtNHX1的植物具有更强的抗逆性和更高的生物量。此外，ZxNHX1在全株水平上控制钠的根系吸收和根到叶的运输，而AtNHX1主要作用于钾的运输过程。我们还在ZxNHX1的一个跨膜区域中鉴定出一个极性残基Thr265，它影响其对钠和钾的选择性。这些发现揭示了一种新的节能型、基于钠的渗透调节机制，该机制可以在不牺牲产量的情况下增强作物的抗逆性，为利用盐碱地将作物生产扩展到边际土地提供了一条有效途径。
