植物响应盐碱胁迫的分子机制研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2024-0410

摘要/Abstract

摘要：

土壤盐碱化是制约全球农业发展的主要环境因素之一。培育耐盐碱作物是应对土壤盐碱化的根本措施，但目前仍面临基因、种质资源匮乏等挑战。挖掘耐盐碱新基因，阐明植物耐盐碱应答的分子机制对培育耐盐碱作物至关重要。盐碱胁迫包括中性盐胁迫和碱性盐胁迫，中性盐胁迫会产生渗透胁迫，Na⁺、Cl^-积累过量还会导致离子毒害，引起氧化胁迫等一系列次生胁迫。与中性盐胁迫相比，碱性盐胁迫还会引起高pH胁迫。论文综述了盐碱胁迫对植物生长发育的影响，总结了近十年植物耐盐碱应答机制的重要研究进展。包括植物对盐胁迫的感知与信号转导，以及植物响应中性盐胁迫和碱性盐胁迫引起的渗透胁迫、离子毒害、氧化胁迫、碳酸氢盐和碳酸盐胁迫、高pH胁迫的分子机制。在此基础上，还讨论了耐盐碱基因在作物育种方面的应用，并提出了提高植物耐盐碱性需要进一步研究的关键科学问题。旨在加深对植物响应盐碱胁迫分子机制的认识，为培育高产、优质的耐盐碱品种及提升盐碱地可开发利用率提供理论基础。

关键词: 盐碱胁迫, 离子毒害, 渗透胁迫, 高pH胁迫, Na⁺转运蛋白, 质膜H⁺-ATPase

Abstract:

Soil salinization is one of a major environmental factor constraining global agricultural development. Breeding saline-alkali tolerant crops is a fundamental strategy to address soil salinization. However, currently there are challenges such as limited saline-alkali-tolerant genes and germplasm resources. Exploring new genes for saline-alkali tolerance and elucidating the molecular mechanisms of plant responses to saline-alkali stress are crucial for developing saline-alkali-tolerant crops. Saline stress includes neutral salt stress and alkaline salt stress. Neutral salt stress induces osmotic stress, and excessive accumulation of Na⁺ and Cl^- may lead to ion toxicity, causing oxidative stress and a series of secondary stresses. Compared to neutral salt stress, alkaline salt stress also induces high pH stress. This review outlines the impact of saline-alkali stress on plant growth and development, as well as the molecular mechanisms underlying plant adaptation to saline-alkali stress and summarizes the significant research progress in plant saline-alkali stress responses over the past decade. It covers plant perception and signal transduction of saline-alkali stress and the molecular mechanisms of plant responses to osmotic stress, ion toxicity, oxidative stress, bicarbonate and carbonate stress, and high pH stress caused by neutral and alkaline salt stress. On this basis, the application of saline-alkali-tolerant genes in crop breeding is also discussed, and key scientific issues that require further research to improve plant saline-alkali tolerance are proposed. The aim of this work is to deepen the understanding of the molecular mechanisms of plant adaptation to saline-alkali stress, providing a theoretical basis for breeding high-yielding and saline-alkali-tolerant crops, and improving the development and utilization rate of salt-affected land.

Key words: saline-alkali stress, ion toxicity, osmotic stress, high pH stress, Na⁺ transporters, plasma membrane H⁺-ATPase

冯凯月, 赵鑫焱, 李子妍, 邱江明, 曹一博. 植物响应盐碱胁迫的分子机制研究进展[J]. 生物技术通报, 2024, 40(10): 122-138.

FENG Kai-yue, ZHAO Xin-yan, LI Zi-yan, QIU Jiang-ming, CAO Yi-bo. Research Advances in the Molecular Mechanisms of Plant Response to Saline-alkali Stress[J]. Biotechnology Bulletin, 2024, 40(10): 122-138.

图/表 4

图1 植物维持离子稳态适应中性盐胁迫的信号通路盐胁迫下，OSCA1和GIPC分别感知外界渗透压和Na+浓度变化，介导Ca2+内流。SOS3与Ca2+结合后与SOS2互作，激活位于质膜上的SOS1促进Na+转运到胞外，SCaBP8和CBL8发挥类似功能。SOS2与AtANN4互作抑制其介导的Ca2+内流。14-3-3λ/κ蛋白和激酶PKS5抑制SOS2的活性。J3、PKS5和14-3-3ω参与调控AHA2的活性。SCaBP8的磷酸化释放其对AKT1的抑制，促进盐胁迫下K+的吸收。位于液泡膜上的NHXs、V H+-ATP酶、CLCs、ZmMATE29分别参与Na+和Cl-的区隔化。14-3-3蛋白通过CPK21依赖与非依赖途径激活K+外流通道GORK，AtPP2CA抑制GORK的活性

Fig. 1 Signaling pathways for homeostasis adaptation in plants under neutral salt stress Under salt stress, OSCA1 and GIPC sense changes in external osmotic pressure and Na+ concentration, respectively, mediating Ca2+ influx. SOS3 binds to Ca2+ and interacts with SOS2, activating SOS1 located on the plasma membrane to promote Na+ transport to the extracellular cell. SCaBP8 and CBL8 perform similar functions. SOS2 interacts with AtANN4 to inhibit its mediation of Ca2+ influx. The 14-3-3λ/κ protein and kinase PKS5 inhibit the activity of SOS2. J3, PKS5, and 14-3-3ω are involved in regulating the activity of AHA2. The phosphorylation of SCaBP8 releases its inhibition of AKT1, promoting K+ uptake under salt stress. NHXs, V H+-ATPase, CLCs, and ZmMATE29 located on the vacuolar membrane are involved in the compartmentalization of Na+ and Cl-, respectively. The 14-3-3 proteins activate the K+ efflux channel GORK through both CPK21-dependent and independent pathway, while AtPP2CA inhibits the activity of GORK

图2 中性盐胁迫下ABA信号介导气孔关闭的分子机制正常条件下，PP2C与SnRK2s蛋白结合，抑制其活性；TOR磷酸化PYR/PYL/RCAR，抑制PYR/PYL/RCAR与ABA结合。渗透胁迫下，PP2C与PYR/PYL/RCAR形成复合物，释放SnRK2s蛋白，激活转录因子AREB/ABF及阴离子通道SLAC1/QUAC1。拟南芥中ABF4激活FYVE1的表达，促进PYR/PYL降解。SnRK2s磷酸化RaptorB可以促进TOR复合物的解离。SnRK2s还可以抑制KAT1的活性，降低细胞膨压，促进气孔闭合

Fig. 2 Molecular mechanism of ABA signaling mediating stomatal closure under neutral salt stress Under normal conditions, PP2C binds to SnRK2s protein and inhibits its activity; TOR phosphorylates PYR/PYL/RCAR and suppresses PYR/PYL/RCAR binding to ABA. Under osmotic stress, PP2C forms a complex with PYR/PYL/RCAR to release SnRK2s protein and activate the transcription factor AREB/ABF and the anion channel SLAC1/QUAC1. ABF4 in Arabidopsis thaliana L. activates the expressions of FYVE1 and promote PYR/PYL degradation. Phosphorylation of RaptorB by SnRK2s promotes the dissociation of the TOR complex. SnRK2s can also inhibit the activity of KAT1, decrease cellular turgor pressure, and promote stomatal closure

图3 中性盐胁迫下离子转运蛋白介导的Na+、K+、Cl-转运和区隔化 Na+通过NSCCs以及高亲和性钾转运蛋白（如OSHKT2;1）进入根表皮细胞，SOS1介导Na+外排。GORK和NSCCs介导盐胁迫下K+外流。HAK5、AKT1介导K+内流。根皮层细胞中，NPF2.5负责Cl-外排，而ZmMATE29和CLCs将Cl-区隔化到液泡中。NHX可能参与调控Na+区隔化到液泡中。盐胁迫诱导 ZmESBL表达水平增加，促进凯氏带发育，抑制Na+通过质外体途径装载到木质部。CIF-GSO1/SGN3-SGN1同样可以增强凯氏带质外体屏障的功能。木质部薄壁细胞中，OsHKT2;1、SOS1介导Na+装载到木质部；HKT1、ZmHAK4和OsHAK12将木质部汁液中的Na+转运到木薄壁细胞。SKOR介导K+装载到木质部导管中；ZmHKT2将K+从木质部导管中去除。NPF2.4和SLAH1/3介导Cl-在木质部导管的装载和卸载

Fig. 3 Ion transporters mediating the transport and compartmentalization of Na+, K+, and Cl- under neutral salt stress Na+ enters the root epidermal cells through NSCCs and high-affinity K+ transporters such as OSHKT2;1, while SOS1 mediates Na+ efflux. GORK and NSCCs mediate K+ efflux under salt stress. HAK5 and AKT1 mediate K+ influx. In root cortex cells, NPF2.5 is responsible for Cl- efflux, while ZmMATE29 and CLCs transports Cl- into the vacuole. NHX might be involved in the regulation of Na+ compartmentalization into the vacuole. Salt stress induces the expressions of ZmESBL increased, promoting CS development and inhibiting Na+ loading into the xylem via the apoplastic pathway. The CIF-GSO1/SGN3-SGN1 pathway can also enhance the function of the apoplastic barrier. In xylem parenchyma cells, Na+ loading into the xylem is mediated by OsHKT2;1 and SOS1. HKT1, ZmHAK4, and OsHAK12 transport Na+ from xylem vessels to parenchyma cells. SKOR mediates K+ loading into the xylem; while ZmHKT2 removes K+ from the xylem. NPF2.4 and SLAH1/3 mediate the loading and unloading of Cl- in the root xylem

图4 植物调节质膜H+-ATP酶活性响应碱性盐胁迫的分子机制小肽（Peps）与其受体（PEPRs）感知胞外pH变化，激活下游信号通路。碱性盐胁迫下，胞质中Ca2+浓度升高，SCaBP3感知Ca2+信号，解除SCaBP3对AHA2的抑制，此外J3可以抑制PKS5对AHA2的抑制。Ca2+与ZmNSA1结合，诱导其通过26S蛋白酶体途径降解，使MHA2和MHA4表达水平上调。MPK级联途径调节盐碱胁迫下PM H+-ATP酶的转录水平和蛋白活性。碱胁迫下TaCCD1和TaSAUR215相互作用，抑制TaPP2C.D1/8对TaHA2的去磷酸化，增强TaHA2的活性

Fig. 4 Molecular mechanism of regulating plasma membrane H+-ATPase activity in plant response to alkaline salt stress Small peptides（Peps）and receptors（PEPRs）sense changes in extracellular pH and activate downstream signaling pathways. Under alkaline salt stress, the cytosolic Ca2+ concentration increases, and SCaBP3 senses the Ca2+ signal and relieves the inhibition of AHA2. Moreover, J3 can inhibit the inhibition of AHA2 by PKS5. Ca2+ binds to ZmNSA1 and induces its degradation through the 26S proteasome pathway, upregulating the expression levels of MHA2 and MHA4. The MPK cascade pathway regulates the transcriptional level and protein activity of PM H+-ATPase under salt stress. Under alkali stress, TaCCD1 and TaSAUR215 interact to inhibit the dephosphorylation of TaPP2C.D1/8 on TaHA2 and enhance the activity of TaHA2

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