Maize DLR1/NHX7 Is Required for Root Development Under Potassium Deficiency.

K+‐deficiency Na+/H+ antiporter lateral root maize

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
23 Oct 2024
Historique:
revised: 19 09 2024
received: 29 05 2024
accepted: 14 10 2024
medline: 24 10 2024
pubmed: 24 10 2024
entrez: 24 10 2024
Statut: aheadofprint

Résumé

Root System Architecture (RSA) is a crucial plant trait that governs a plant's ability to absorb water and nutrients. In this study, we describe a mutant with nutrient-dependent defects in root development, affecting both the primary root and lateral roots (LRs). This mutant, identified through a screen for defects in LR development, has been designated dlr1-1. The dlr1-1 mutant exhibits impaired LR emergence rather than defects in the LR primordium (LRP) formation, particularly under potassium (K

Identifiants

pubmed: 39444137
doi: 10.1111/pce.15246
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : This work was financially supported by the National Key R&D Program of China (No. 2023YFA0914600 and 2022YFF1001700), the National Natural Science Foundation of China (No. 32360511 and 32400251), the Natural Science Foundation of Henan Province (242300421026, 222300420026 and 222301420103), the Zhongyuan Scholar Workstation Funding Program (244400510016), the Hainan Provincial Joint Project of Sanya Yazhou Bay Science and Technology City (No. 2021JJLH0008 and No. 2021JJLH0044), and the Henan Provincial Higher Education Key Research Project Program (No. 24A180006).

Informations de copyright

© 2024 John Wiley & Sons Ltd.

Références

Acharya, B. R., C. Zhao, L. A. R. Reyes, J. F. S. Ferreira, and D. Sandhu. 2023. “Understanding the Salt Overly Sensitive Pathway in Prunus: Identification and Characterization of NHX, CIPK, and CBL Genes.” Plant Genome 17, no. 1: e20371.
Adams, E., and R. Shin. 2014. “Transport, Signaling, and Homeostasis of Potassium and Sodium in Plants.” Journal of Integrative Plant Biology 56, no. 3: 231–249.
Ali, A., V. Petrov, D. J. Yun, and T. Gechev. 2023. “Revisiting Plant Salt Tolerance: Novel Components of the SOS Pathway.” Trends in Plant Science 28, no. 9: 1060–1069.
Armengaud, P., R. Breitling, and A. Amtmann. 2004. “The Potassium‐Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling.” Plant Physiology 136, no. 1: 2556–2576.
Assaha, D. V. M., A. Ueda, H. Saneoka, R. Al‐Yahyai, and M. W. Yaish. 2017. “The Role of Na and K Transporters in Salt Stress Adaptation in Glycophytes.” Frontiers in Physiology 8: 509.
Bagautdinova, Z. Z., N. Omelyanchuk, A. V. Tyapkin, V. V. Kovrizhnykh, V. V. Lavrekha, and E. V. Zemlyanskaya. 2022. “Salicylic Acid in Root Growth and Development.” International Journal of Molecular Sciences 23, no. 4: 2228.
Cao, Y., M. Zhang, X. Liang, et al. 2020. “Natural Variation of an EF‐Hand Ca(2+)‐Binding‐Protein Coding Gene Confers Saline‐Alkaline Tolerance in Maize.” Nature Communications 11, no. 1: 186.
Chen, G., H. Feng, Q. Hu, et al. 2015. “Improving Rice Tolerance to Potassium Deficiency by Enhancing OsHAK16p:WOX11‐Controlled Root Development.” Plant Biotechnology Journal 13, no. 6: 833–848.
Cui, J., M. Nieves‐Cordones, F. Rubio, and G. Tcherkez. 2021. “Involvement of Salicylic Acid in the Response to Potassium Deficiency Revealed by Metabolomics.” Plant Physiology and Biochemistry 163: 201–204.
Ding, L., and J. K. Zhu. 1997. “Reduced Na+ Uptake in the NaCl‐Hypersensitive SOS1 Mutant of Arabidopsis thaliana.” Plant Physiology 113, no. 3: 795–799.
Echevarría‐Machado, I., R. M. Escobedo‐G.m., and A. Larqué‐Saavedra. 2007. “Responses of Transformed Catharanthus roseus Roots to Femtomolar Concentrations of Salicylic Acid.” Plant Physiology and Biochemistry 45, no. 6–7: 501–507.
Giehl, R. F. H., B. D. Gruber, and N. von Wirén. 2014. “It's Time to Make Changes: Modulation of Root System Architecture by Nutrient Signals.” Journal of Experimental Botany 65, no. 3: 769–778.
Halfter, U., M. Ishitani, and J. K. Zhu. 2000. “TheArabidopsis SOS2 Protein Kinase Physically Interacts With and Is Activated by the Calcium‐Binding Protein SOS3.” Proceedings of the National Academy of Sciences 97, no. 7: 3735–3740.
Hasanuzzaman, M., M. Bhuyan, K. Nahar, et al. 2018. “Potassium: A Vital Regulator of Plant Responses and Tolerance to Abiotic Stresses.” Agronomy 8, no. 3: 31.
He, J., H. Dai, X. Zhang, and E. Wang. 2024. “Mycorrhizal Signals Promote Root Development Dependent on LysM‐Receptor Like Kinases in Rice.” New Crops 1: 100009.
Hussain, S., S. Hussain, B. Ali, et al. 2021. “Recent Progress in Understanding Salinity Tolerance in Plants: Story of Na/K Balance and Beyond.” Plant Physiology and Biochemistry 160: 239–256.
Ji, H., J. M. Pardo, G. Batelli, M. J. Van Oosten, R. A. Bressan, and X. Li. 2013. “The Salt Overly Sensitive (SOS) Pathway: Established and Emerging Roles.” Molecular Plant 6, no. 2: 275–286.
Jia, Z., R. F. H. Giehl, and N. von Wirén. 2022. “Nutrient‐Hormone Relations: Driving Root Plasticity in Plants.” Molecular Plant 15, no. 1: 86–103.
Jia, Z., and N. von Wirén. 2020. “Signaling Pathways Underlying Nitrogen‐Dependent Changes in Root System Architecture: From Model to Crop Species.” Journal of Experimental Botany 71, no. 15: 4393–4404.
Jiang, L., B. Yao, X. Zhang, et al. 2023. “Salicylic Acid Inhibits Rice Endocytic Protein Trafficking Mediated by OsPIN3t and Clathrin to Affect Root Growth.” The Plant Journal 115, no. 1: 155–174.
Johnson, R., K. Vishwakarma, M. S. Hossen, et al. 2022. “Potassium in Plants: Growth Regulation, Signaling, and Environmental Stress Tolerance.” Plant Physiology and Biochemistry 172: 56–69.
Jung, J.‐Y., R. Shin, and D. P. Schachtman. 2009. “Ethylene Mediates Response and Tolerance to Potassium Deprivation in Arabidopsis.” The Plant Cell 21, no. 2: 607–621.
Kotogány, E., D. Dudits, G. V. Horváth, and F. Ayaydin. 2010. “A Rapid and Robust Assay for Detection of S‐Phase Cell Cycle Progression in Plant Cells and Tissues by Using Ethynyl Deoxyuridine.” Plant Methods 6, no. 1: 5.
Kumar, P., T. Kumar, S. Singh, N. Tuteja, R. Prasad, and J. Singh. 2020. “Potassium: A Key Modulator for Cell Homeostasis.” Journal of Biotechnology 324: 198–210.
Li, A., X. Sun, and L. Liu. 2022. “Action of Salicylic Acid on Plant Growth.” Frontiers in Plant Science 13: 878076.
Li, J., L. Shen, X. Han, et al. 2023. “Phosphatidic Acid‐Regulated SOS2 Controls Sodium and Potassium Homeostasis in Arabidopsis Under Salt Stress.” The EMBO Journal 42, no. 8: e112401.
Li, X., R. Zeng, and H. Liao. 2016. “Improving Crop Nutrient Efficiency Through Root Architecture Modifications.” Journal of Integrative Plant Biology 58, no. 3: 193–202.
Lin, H., Y. Yang, R. Quan, et al. 2009. “Phosphorylation of SOS3‐LIKE Calcium Binding PROTEIN8 by SOS2 Protein Kinase Stabilizes Their Protein Complex and Regulates Salt Tolerance in.” Plant Cell 21, no. 5: 1607–1619.
Liu, Z., C. Ma, L. Hou, et al. 2022. “Exogenous SA Affects Rice Seed Germination Under Salt Stress by Regulating Na+/K+ Balance and Endogenous GAs and ABA Homeostasis.” International Journal of Molecular Sciences 23, no. 6: 3293.
Luo, M., Y. Zhao, Y. Zhang, et al. (2022). A 4‐bp Natural Deletion of Maize Na+/H+ Exchanger Gene Alters Maize Salt Stress Tolerance.
Lv, X., Y. Zhang, L. Hu, et al. 2021. “Low‐Nitrogen Stress Stimulates Lateral Root Initiation and Nitrogen Assimilation in Wheat: Roles of Phytohormone Signaling.” Journal of Plant Growth Regulation 40, no. 1: 436–450.
Mostofa, M. G., M. M. Rahman, T. K. Ghosh, et al. 2022. “Potassium in Plant Physiological Adaptation to Abiotic Stresses.” Plant Physiology and Biochemistry 186: 279–289.
Pasternak, T., E. P. Groot, F. V. Kazantsev, et al. 2019. “Salicylic Acid Affects Root Meristem Patterning via Auxin Distribution in a Concentration‐Dependent Manner.” Plant Physiology 180, no. 3: 1725–1739.
Pélissier, P.‐M., H. Motte, and T. Beeckman. 2021. “Lateral Root Formation and Nutrients: Nitrogen in the Spotlight.” Plant Physiology 187, no. 3: 1104–1116.
Peng, Y., J. Yang, X. Li, and Y. Zhang. 2021. “Salicylic Acid: Biosynthesis and Signaling.” Annual Review of Plant Biology 72, no. 1: 761–791.
Qi, Z., and E. P. Spalding. 2004. “Protection of Plasma Membrane K+ Transport by the Salt Overly Sensitive1 Na+‐H+ Antiporter During Salinity Stress.” Plant Physiology 136, no. 1: 2548–2555.
Qin, Y. J., W. H. Wu, and Y. Wang. 2019. “ZmHAK5 and ZmHAK1 Function in K Uptake and Distribution in Maize Under Low K Conditions.” Journal of Integrative Plant Biology 61, no. 6: 691–705.
Quan, R., H. Lin, I. Mendoza, et al. 2007. “SCABP8/CBL10, a Putative Calcium Sensor, Interacts With the Protein Kinase SOS2 to Protectarabidopsisshoots From Salt Stress.” Plant Cell 19, no. 4: 1415–1431.
Quintero, F. J., J. Martinez‐Atienza, I. Villalta, et al. 2011. “Activation of the Plasma Membrane Na/H Antiporter Salt‐Overly‐Sensitive 1 (SOS1) by Phosphorylation of an Auto‐Inhibitory C‐Terminal Domain.” Proceedings of the National Academy of Sciences 108, no. 6: 2611–2616.
Quintero, F. J., M. Ohta, H. Shi, J. K. Zhu, and J. M. Pardo. 2002. “Reconstitution in Yeast of the Arabidopsis SOS Signaling Pathway for Na+ Homeostasis.” Proceedings of the National Academy of Sciences 99, no. 13: 9061–9066.
Ren, M., Y. Li, J. Zhu, K. Zhao, Z. Wu, and C. Mao. 2023. “Phenotypes and Molecular Mechanisms Underlying the Root Response to Phosphate Deprivation in Plants.” International Journal of Molecular Sciences 24, no. 6: 5107.
Rodríguez‐Navarro, A., and J. Ramos. 1984. “Dual System for Potassium Transport in Saccharomyces cerevisiae.” Journal of Bacteriology 159, no. 3: 940–945.
Santos Teixeira, J. A., and K. H. ten Tusscher. 2019. “The Systems Biology of Lateral Root Formation: Connecting the Dots.” Molecular Plant 12, no. 6: 784–803.
Sawada, H., I.‐S. Shim, and K. Usui. 2006. “Induction of Benzoic Acid 2‐Hydroxylase and Salicylic Acid Biosynthesis—Modulation by Salt Stress in Rice Seedlings.” Plant Science 171, no. 2: 263–270.
Schachtman, D. P. 2015. “The Role of Ethylene in Plant Responses to K Deficiency.” Frontiers in Plant Science 6: 1153.
Shakirova, F. M., A. R. Sakhabutdinova, M. V. Bezrukova, R. A. Fatkhutdinova, and D. R. Fatkhutdinova. 2003. “Changes in the Hormonal Status of Wheat Seedlings Induced by Salicylic Acid and Salinity.” Plant Science 164, no. 3: 317–322.
Shin, R., R. H. Berg, and D. P. Schachtman. 2005. “Reactive Oxygen Species and Root Hairs in Arabidopsis Root Response to Nitrogen, Phosphorus and Potassium Deficiency.” Plant and Cell Physiology 46, no. 8: 1350–1357.
Shin, R., A. Y. Burch, K. A. Huppert, et al. 2007. “The Arabidopsis Transcription Factor MYB77 Modulates Auxin Signal Transduction.” Plant Cell 19, no. 8: 2440–2453.
Shin, R., and D. P. Schachtman. 2004. “Hydrogen Peroxide Mediates Plant Root Cell Response to Nutrient Deprivation.” Proceedings of the National Academy of Sciences 101, no. 23: 8827–8832.
Song, W., S. Liu, L. Meng, et al. 2015. “Potassium Deficiency Inhibits Lateral Root Development in Tobacco Seedlings by Changing Auxin Distribution.” Plant and Soil 396, no. 1–2: 163–173.
Spoel, S. H., and X. Dong. 2024. “Salicylic Acid in Plant Immunity and Beyond.” Plant Cell 36, no. 5: 1451–1464.
Sun, C. H., J. Q. Yu, and D. G. Hu. 2017. “Nitrate: A Crucial Signal During Lateral Roots Development.” Frontiers in Plant Science 8: 485.
Tan, S., M. Abas, I. Verstraeten, et al. 2020. “Salicylic Acid Targets Protein Phosphatase 2A to Attenuate Growth in Plants.” Current Biology 30, no. 3: 381–395.e8.
Thordal‐Christensen, H., Z. Zhang, Y. Wei, and D. B. Collinge. 2002. “Subcellular Localization of H2O2 in Plants. H2O2 Accumulation in Papillae and Hypersensitive Response During the Barley—Powdery Mildew Interaction.” Plant Journal 11, no. 6: 1187–1194.
Tian, H., I. De Smet, and Z. Ding. 2014. “Shaping a Root System: Regulating Lateral Versus Primary Root Growth.” Trends in Plant Science 19, no. 7: 426–431.
Wang, Y., R. Wang, S. Zhao, C. Lu, Z. Zhu, and H. Li. 2022. “Transporter NRT1.5/NPF7.3 Suppresses Primary Root Growth Under Low K Stress by Regulating the Degradation of PIN‐FORMED2.” BMC Plant Biology 22, no. 1: 330.
Wang, Y., and W.‐H. Wu. 2017. “Regulation of Potassium Transport and Signaling in Plants.” Current Opinion in Plant Biology 39: 123–128.
Wu, C., X. Wang, W. Zhen, et al. 2022. “Sickle Modulates Lateral Root Development by Promoting Degradation of Lariat Intronic Rna.” Plant Physiology 190, no. 1: 548–561.
Wu, C., W. Zhen, X. Wang, Y. Li, W. Wang, and Z. Hu. 2023. “Absence of Sickle Triggers Programed Cell Death by Disturbing Alternative Splicing and Decay of mRNAs.” Plant Physiology 192, no. 3: 2523–2536.
Yamauchi, T., A. Tanaka, H. Inahashi, et al. 2019. “Fine Control of Aerenchyma and Lateral Root Development Through AUX/IAA‐ and ARF‐Dependent Auxin Signaling.” Proceedings of the National Academy of Sciences 116, no. 41: 20770–20775.
Yang, J., H. Zhang, and J. Zhang. 2012. “Root Morphology and Physiology in Relation to the Yield Formation of Rice.” Journal of Integrative Agriculture 11, no. 6: 920–926.
Yang, Y., and Y. Guo. 2018. “Unraveling Salt Stress Signaling in Plants.” Journal of Integrative Plant Biology 60, no. 9: 796–804.
Zhang, M., Y. Cao, Z. Wang, et al. 2018. “A Retrotransposon in an HKT1 Family Sodium Transporter Causes Variation of Leaf Na(+) Exclusion and Salt Tolerance in Maize.” New Phytologist 217, no. 3: 1161–1176.
Zhang, M. L., P. P. Huang, Y. Ji, et al. 2020. “KUP9 Maintains Root Meristem Activity by Regulating K and Auxin Homeostasis in Response to Low K.” EMBO Reports 21, no. 6: e50164.
Zhang, Y., X. Duan, Y. Xie, and W. Xuan. 2024. “Uncovering the Function of Peptides: Bridging Hormone Signaling, Microbial Interactions, and Root Development in Plants.” New Crops 1: 100011.
Zhou, H., H. Ge, J. Chen, et al. 2022. “Salicylic Acid Regulates Root Gravitropic Growth via Clathrin‐Independent Endocytic Trafficking of PIN2 Auxin Transporter in Arabidopsis thaliana.” International Journal of Molecular Sciences 23, no. 16: 9379.
Zhou, X., J. Li, Y. Wang, et al. 2022. “The Classical SOS Pathway Confers Natural Variation of Salt Tolerance in Maize.” New Phytologist 236, no. 2: 479–494.

Auteurs

Kang Guo (K)

The Zhongzhou Laboratory for Integrative Biology, State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China.

Daojun Li (D)

The Zhongzhou Laboratory for Integrative Biology, State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China.

Yan Li (Y)

The Zhongzhou Laboratory for Integrative Biology, State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China.

Xiaoqing Wang (X)

The Zhongzhou Laboratory for Integrative Biology, State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China.

Chunfei Wang (C)

The Zhongzhou Laboratory for Integrative Biology, State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China.

Yanbin Zhu (Y)

The Zhongzhou Laboratory for Integrative Biology, State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China.
Sanya Institute, Henan University, Sanya, China.

Chengyun Wu (C)

The National Engineering Lab of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural University, Hefei, China.

Zhubing Hu (Z)

The Zhongzhou Laboratory for Integrative Biology, State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China.
Sanya Institute, Henan University, Sanya, China.

Classifications MeSH