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The Nascent Polypeptide-Associated Complex Subunit Alpha-Like Protein 1 (PmNACA1) Enhances Drought Tolerance by Scavenging ROS in Prunus mira Koehne

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Abstract

Extreme environmental stress significantly impacts plant growth. Drought stress is one of the most important abiotic stresses, adversely affecting plant development and agricultural productivity. Prunus mira is an exceptionally drought-tolerant plant. However, there are a limited number studies on the drought resistance of it. Here, we isolated and identified nascent polypeptide-associated complex subunit alpha-like protein 1 of P. mira (PmNACA1). PmNACA1 comprises 201 amino acids and contains an NAC domain at its N-terminal. It was localized in the cytoplasm and nucleus. PmNACA1 was primarily expressed in leaves, and was induced by drought. PmNACA1 overexpression Arabidopsis thaliana increased germination and root elongation. Histochemical staining revealed that the overexpression lines accumulated less ROS under mannitol-induced osmotic stress. Under drought stress, overexpression lines exhibited an elevation in the activities of SOD, POD, CAT, and GR and a rise in the levels of GSH and GSSG. In addition, the overexpression lines exhibited relatively lower levels of H2O2, O2.−, MDA, and electrical conductivity than control plants. PmNACA1 induced the expression of drought- and ABA-related genes after drought treatment. PmNACA1 scavenged H2O2, DPPH radicals, and hydroxyl radicals in vitro. In summary, we conclude that PmNACA1 plays an active role in drought stress response by scavenging ROS.

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Data Availability Statement

All data supporting the findings of this study are available within the paper and within its supplementary materials published online.

References

  • Baldoni E, Genga A, Cominelli E (2015) Plant MYB transcription factors: their role in drought response mechanisms. Int J Mol Sci IJMS 16:15811–15851. https://doi.org/10.3390/ijms160715811

    Article  CAS  PubMed  Google Scholar 

  • Bhatt M, Pandey SS, Tiwari AK, Tiwari BS (2021) Plastid mediated singlet oxygen in regulated cell death. Plant Biol. https://doi.org/10.1111/plb.13260

    Article  PubMed  Google Scholar 

  • Cao Y, Luo Q, Tian Y, Meng F (2017) Physiological and proteomic analyses of the drought stress response in Amygdalus Mira (Koehne) Yu et Lu roots. BMC Plant Biol 17(1):53

    PubMed  PubMed Central  Google Scholar 

  • Celik I, Isik I (2008) Determination of chemopreventive role of Foeniculum vulgare and Salvia officinalis infusion on trichloroacetic acid-induced increased serum marker enzymes lipid peroxidation and antioxidative defense systems in rats. Nat Prod Res 22(1):66–75

    CAS  PubMed  Google Scholar 

  • Chen K, Su C, Tang W, Zhou Y, Xu Z, Chen J, Li H, Chen M, Ma Y (2021) Nuclear transport factor GmNTF2B-1 enhances soybean drought tolerance by interacting with oxidoreductase GmOXR17 to reduce reactive oxygen species content. Plant J 107(3):740–759

    CAS  PubMed  Google Scholar 

  • del Alamo M, Hogan DJ, Pechmann S, Albanese V, Brown PO, Frydman J (2011) Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol 9(7):23

    Google Scholar 

  • Ding Y, Jia Y, Shi Y, Zhang X, Song C, Gong Z, Yang S (2018) OST1-mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses. EMBO J https://doi.org/10.15252/embj.201798228

  • Ezatollah ESFANDIARI, Gholamreza GOHARI (2017) Response of ROS-scavenging systems to salinity stress in two different wheat (Triticum aestivum L.) Cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 45(1):287–291

    Google Scholar 

  • Fila J, Klodova B, Potesil D, Juricek M, Sestak P, Zdrahal Z, Honys D (2020) The beta subunit of nascent polypeptide associated complex plays a role in flowers and siliques development of Arabidopsis thaliana. Int J Mol Sci 21(6):30

    Google Scholar 

  • Gechev T, Petrov V (2020) Reactive oxygen species and abiotic stress in plants. Int J Mol Sci 21(20):5

    Google Scholar 

  • George R, Walsh P, Beddoe T, Lithgow T (2002) The nascent polypeptide-associated complex (NAC) promotes interaction of ribosomes with the mitochondrial surface in vivo. FEBS Lett 516(1–3):213–216

    CAS  PubMed  Google Scholar 

  • Guan C, Ji J (2014) LcKRP, a cyclin-dependent kinase inhibitor from Lycium chinense, is involved in an ABA-dependent drought stress-signaling pathway. Plant Soil. https://doi.org/10.1007/s11104-014-2134-5

    Article  Google Scholar 

  • Ha Y, Shang Y, Nam KH (2016) Brassinosteroids modulate ABA-induced stomatal closure in Arabidopsis. J Exp Bot 67(22):6297–6308

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hao D, Fei H, Wu N, Li X, **ong L (2018) Integrative regulation of drought escape through ABA dependent and independent pathways in rice. Mol Plant 11(4):584

    Google Scholar 

  • Hasanuzzaman M, Alam MM, Nahar K, Fujita M (2014) Trehalose-induced drought stress tolerance: a comparative study among different Brassica species. Plant Omics 7(4):271–283

    Google Scholar 

  • He F, Wang HL, Li HG, Su Y, Li S, Yang Y, Feng CH, Yin W, **a X (2018) PeCHYR1, a ubiquitin E3 ligase from Populus euphratica, enhances drought tolerance via ABA-induced stomatal closure by ROS production in Populus. Plant Biotechnol J 16(8):1514–1528

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hissin PJ, Hilf R (1976) A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 74(1):214–226

    CAS  PubMed  Google Scholar 

  • Hossain MS, Li J, Sikdar A, Hasanuzzaman M, Uzizerimana F, Muhammad I, Yuan Y, Zhang C, Wang C, Feng B (2020) Exogenous melatonin modulates the physiological and biochemical mechanisms of drought tolerance in tartary buckwheat (Fagopyrum tataricum (L) Gaertn). Molecules 25(12):2828

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jamil M, Wang WY, Xu MY, Tu JM (2015) Exploring the roles of basal transcription factor 3 in eukaryotic growth and development, In Mayes S (ed), Biotechnology and Genetic Engineering Reviews, Vol 31, Issue 1–2, Ed, Routledge, Abingdon pp 21–45

  • Jia DF, Jiang Q, van Nocker S, Gong XQ, Ma FW (2019) An apple (Malus domestica) NAC transcription factor enhances drought tolerance in transgenic apple plants. Plant Physiol Biochem 139:504–512

    CAS  PubMed  Google Scholar 

  • Ju YL, Min Z, Yue XF, Zhang YL, Zhang JX, Zhang ZQ, Fang YL (2020) Overexpression of grapevine VvNAC08 enhances drought tolerance in transgenic Arabidopsis. Plant Physiol Biochem 151:214–222

    CAS  PubMed  Google Scholar 

  • Kaliyugam, Shiriga, Rinku, Sharma, Krishan, Kumar, Shiv, Kumar, Yadav, Firoz (2014) Genome-wide identification and expression pattern of drought-responsive members of the NAC family in maize. Meta Gene

  • Karan R, Subudhi PK (2012) Overexpression of a nascent polypeptide associated complex gene (SaβNAC) of Spartina alterniflora improves tolerance to salinity and drought in transgenic Arabidopsis. Biochem Biophys Res Commun 424(4):747–752

    CAS  PubMed  Google Scholar 

  • Kazuo N, Kazuko Y-S (2013) ABA signaling in stress-response and seed development. Plant Cell Rep. https://doi.org/10.1007/s00299-013-1418-1

    Article  Google Scholar 

  • Kumar K, Muthamilarasan M, Bonthala VS, Roy R, Prasad M (2015) Subcellular localization of candidate Si14–3–3 proteins in onion epidermal cells

  • Kurkela S, Borg-Franck M (1992) Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19(4):689–692

    CAS  PubMed  Google Scholar 

  • Lee K, Han KS, Kwon YS, Lee JH, Kim SH, Chung WS, Kim Y, Chun SS, Kim HK, Bae DW (2009) Identification of potential DREB2C targets in Arabidopsis thaliana plants overexpressing DREB2C using proteomic analysis. Mol Cells 28(4):383–388

    CAS  PubMed  Google Scholar 

  • Lei P, Liu Z, Li J, ** G, Xu L, Ji X, Zhao X, Tao L, Meng F (2022) Integration of the physiology, transcriptome and proteome reveals the molecular mechanism of drought tolerance in Cupressus gigantea. Forests 13(3):401

    Google Scholar 

  • Li SX, **e JC, Yang X, Xue RH, Zhao PY (2022) The dynamic identification mechanism research of drought based on process description. Water Supply 22(9):7281–7296

    Google Scholar 

  • Liu JJ, Wei Z, Li JH (2014) Effects of copper on leaf membrane structure and root activity of maize seedling. Bot Stud 55:6

    CAS  Google Scholar 

  • Liu X, Wang L, Cui H, Zhu H, Bi S, Zhang Z, Meng S, Song C, Wang H, Ma F (2019) Effects of magnetic treatment on the ascorbate–glutathione cycle and endogenous hormone levels in Populus × euramericana ‘Neva’ under cadmium stress. Canadian J Forest Res 49:1147

    CAS  Google Scholar 

  • Mao H, Li S, Chen B, Jian C, Mei F, Zhang Y, Li F, Chen N, Li T, Du L, Ding L, Wang Z, Cheng X, Wang X, Kang Z (2022) Variation in cis-regulation of a NAC transcription factor contributes to drought tolerance in wheat. Mol Plant 15(2):276–292

    CAS  PubMed  Google Scholar 

  • Meng YC, Zhang HF, Pan XX, Chen N, Chen R (2021) CaDHN3, a pepper (Capsicum annuum L.) Dehydrin gene enhances the tolerance against salt and drought stresses by reducing ROS accumulation. Int J Mol Sci 22(6):3205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morris D, Gostick JT (2012) Determination of the in-plane components of the electrical conductivity tensor in PEM fuel cell gas diffusion layers. Electrochim Acta 85:665

    CAS  Google Scholar 

  • Msanne J, Lin JS, Stone JM, Awada T (2011) Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234(1):97–107

    CAS  PubMed  Google Scholar 

  • Palta JP, Stadelmann EJ (2010) On simultaneous transport of water and solute through plant cell membranes: evidence for the absence of solvent drag effect and insensitivity of the reflection coefficient. Physiol Plant 50(1):83–90

    Google Scholar 

  • Park HL, Cho M-H, Shin DH, Bhoo SH, Hahn T-R (2012) Molecular characterization of phytochrome-interacting nascent polypeptide associated complex protein in Arabidopsis thaliana. J Korean Soc Appl Biol Chem 55(2):323–326

    CAS  Google Scholar 

  • Ponce-Rojas JC, Avendano-Monsalve MC, Yanez-Falcon AR, Jaimes-Miranda F, Garay E, Torres-Quiroz F, DeLuna A, Funes S (2017) alpha beta’-NAC cooperates with Sam37 to mediate early stages of mitochondrial protein import. Febs J 284(5):814–830

    CAS  PubMed  Google Scholar 

  • Reimann B, Bradsher J, Franke J, Hartmann E, Wiedmann M, Prehn S, Wiedmann B (1999) Initial characterization of the nascent polypeptide-associated complex in yeast. Yeast (chichester, England) 15(5):397–407

    CAS  PubMed  Google Scholar 

  • Souza TCd, Magalhães PC, Castro EMD, Carneiro NP, Júnior CCG (2014) ABA application to maize hybrids contrasting for drought tolerance: changes in water parameters and in antioxidant enzyme activity. Plant Growth Regul 73(3):205–217

    Google Scholar 

  • Thalmann M (2017) The function and regulation of starch degradation during plant responses to abiotic stress

  • Than W, Qin F, Liu W, Wang X (2016) Analysis of Sogatella furcifera proteome that interact with P10 protein of Southern rice black-streaked dwarf virus. Sci Rep 6:32445

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tong S, Chen N, Wang D, Ai F, Liu B, Ren L, Chen Y, Zhang J, Lou S, Liu H (2021) The U-box E3 ubiquitin ligase PalPUB79 positively regulates ABA-dependent drought tolerance via ubiquitination of PalWRKY77 in Populus. Plant Biotechnol J 19(12):2561–2575

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JG, Zhang CL (2000) The inhibition of DNA synthesis induced by ROS and drought resistivity of wheat. Acta Botan Boreali-Occiden Sin 20(3):376–381

    CAS  Google Scholar 

  • Wang X, Liu S, Zuo H, Zheng W, Zhang S, Huang Y, **cuo G, Ying H, Zhao F, Li Y, Liu J, Yi TS, Zan Y, Larkin RM, Deng X, Zeng X, Xu Q (2021) Genomic basis of high-altitude adaptation in Tibetan Prunus fruit trees. Curr Biol. https://doi.org/10.1016/j.cub.2021.06.062

    Article  PubMed  PubMed Central  Google Scholar 

  • Wegrzyn RD, Hofmann D, Merz F, Nikolay R, Rauch T, Graf C, Deuerling E (2006) A conserved motif is prerequisite for the interaction of NAC with ribosomal protein L23 and nascent chains. J Biol Chem 281(5):2847–2857

    CAS  PubMed  Google Scholar 

  • Wiedmann B, Prehn S (1999) The nascent polypeptide-associated complex (NAC) of yeast functions in the targeting process of ribosomes to the ER membrane. FEBS Lett 458(1):51–54

    CAS  PubMed  Google Scholar 

  • Windarti CK, Maryanto AE, Salamah A, Andayani N (2021) The study of Heat shock protein 70 (Hsp70) gene expression on Ageratum conyzoides L. and Synedrella nodiflora L. in Universitas Indonesia, Depok and Cibodas Botanical Garden. J Phys Conference Series 1725(1):012059

    CAS  Google Scholar 

  • Wunna H, Jogloy S, Toomsan B (2009) Traits related to nitrogen fixation, yield and drought tolerance in peanut (Amchis hypogaea L.) Under Early Drought.

  • Xu L, Hu Y, ** G, Lei P, Sang L, Luo Q, Liu Z, Guan F, Meng F, Zhao X (2021) Physiological and proteomic responses to drought in leaves of Amygdalus mira (Koehne) Yu et Lu. Front Plant Sci. https://doi.org/10.3389/fpls.2021.620499

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5(1):235–244

    CAS  PubMed  Google Scholar 

  • Yan J, Tsuichihara N, Etoh T, Iwai S (2007) Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening. Plant Cell Environ 30(10):1320–1325

    CAS  PubMed  Google Scholar 

  • Yang KS, Kim HS, ** UH, Lee SS, Park JA, Lim YP, Pai HS (2007) Silencing of NbBTF3 results in developmental defects and disturbed gene expression in chloroplasts and mitochondria of higher plants. Planta 225(6):1459–1469

    CAS  PubMed  Google Scholar 

  • Zhao CC, Huang FD, Pan G, Yang X, Cheng FM, Pan G (2014) Physiological characteristics and gene map** of a leaf early-senescence mutant osled in rice. Acta Agronomica Sinica 40(11):1946

  • Zhao N, He M, Li L, Cui S, Yang X (2020) Identification and expression analysis of WRKY gene family under drought stress in peanut (Arachis hypogaea L). PLoS ONE 15(4):e0231396

    CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was funded by the Fundamental Research Funds for the Central Universities (2572018CG05); the National Natural Science Foundation of China (No. 31760548, No. 31760548); Guangxi Natural Science Foundation under Grant No. 2022JIA130042: Molecular regulation of flower development and nervonic acid synthesis in Malania oleifera; Baise Science and Technology Development Funds (BS2022002): Identification and Conservation of endangered medicinal plant resources of Baise.

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Authors and Affiliations

  1. College of Life Science, Northeast Forestry University, Harbin, 150040, China

    Jianxin Li, Qiuxiang Luo & Fanjuan Meng

  2. State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China

    Jianxin Li, Subin Zhang, Pei Lei & Fanjuan Meng

  3. School of Laboratory Medicine, Youjiang Medical University for Nationalities, Baise, 533000, China

    Qijiang Xu

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  1. Jianxin Li
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Li, J., Zhang, S., Lei, P. et al. The Nascent Polypeptide-Associated Complex Subunit Alpha-Like Protein 1 (PmNACA1) Enhances Drought Tolerance by Scavenging ROS in Prunus mira Koehne. J. Plant Biol. 67, 137–152 (2024). https://doi.org/10.1007/s12374-023-09418-0

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