Overexpression of PavHIPP16 from Prunus avium enhances cold stress tolerance in transgenic tobacco.


Journal

BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807

Informations de publication

Date de publication:
12 Jun 2024
Historique:
received: 15 01 2024
accepted: 07 06 2024
medline: 12 6 2024
pubmed: 12 6 2024
entrez: 11 6 2024
Statut: epublish

Résumé

The heavy metal-associated isoprenylated plant protein (HIPP) is an important regulatory element in response to abiotic stresses, especially playing a key role in low-temperature response. This study investigated the potential function of PavHIPP16 up-regulated in sweet cherry under cold stress by heterologous overexpression in tobacco. The results showed that the overexpression (OE) lines' growth state was better than wild type (WT), and the germination rate, root length, and fresh weight of OE lines were significantly higher than those of WT. In addition, the relative conductivity and malondialdehyde (MDA) content of the OE of tobacco under low-temperature treatment were substantially lower than those of WT. In contrast, peroxidase (POD), superoxide dismutase (SOD), catalase (CAT) activities, hydrogen peroxide (H This study provides genetic resources for analyzing the biological functions of PavHIPPs, which is important for elucidating the mechanisms of cold resistance in sweet cherry.

Sections du résumé

BACKGROUND BACKGROUND
The heavy metal-associated isoprenylated plant protein (HIPP) is an important regulatory element in response to abiotic stresses, especially playing a key role in low-temperature response.
RESULTS RESULTS
This study investigated the potential function of PavHIPP16 up-regulated in sweet cherry under cold stress by heterologous overexpression in tobacco. The results showed that the overexpression (OE) lines' growth state was better than wild type (WT), and the germination rate, root length, and fresh weight of OE lines were significantly higher than those of WT. In addition, the relative conductivity and malondialdehyde (MDA) content of the OE of tobacco under low-temperature treatment were substantially lower than those of WT. In contrast, peroxidase (POD), superoxide dismutase (SOD), catalase (CAT) activities, hydrogen peroxide (H
CONCLUSIONS CONCLUSIONS
This study provides genetic resources for analyzing the biological functions of PavHIPPs, which is important for elucidating the mechanisms of cold resistance in sweet cherry.

Identifiants

pubmed: 38862890
doi: 10.1186/s12870-024-05267-2
pii: 10.1186/s12870-024-05267-2
doi:

Substances chimiques

Plant Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

536

Subventions

Organisme : the National Natural Science Foundation of China
ID : Grant No. 32160700
Organisme : he Guizhou Provincial Science and Technology Projects of China
ID : Grant No. YQK[2023]008
Organisme : the National Guidance of Local Science and Technology Development Fund of China
ID : Grant No. [2023]009
Organisme : the Guizhou Provincial Science and Technology Projects of China
ID : Grant No. [2021] Yiban231

Informations de copyright

© 2024. The Author(s).

Références

Zhang H, Zhang X, Liu J, Niu Y, Chen Y, Hao Y et al. Characterization of the heavy-metal-associated isoprenylated plant protein (HIPP) gene family from triticeae species. Int J Mol Sci. 2020;21.
Bull PC, Cox DW. Wilson disease and Menkes disease: new handles on heavy-metal transport. Trends Genet. 1994;10:246–52.
pubmed: 8091505 doi: 10.1016/0168-9525(94)90172-4
Barth O, Vogt S, Uhlemann R, Zschiesche W, Humbeck K. Stress induced and nuclear localized HIPP26 from Arabidopsis thaliana interacts via its heavy metal associated domain with the drought stress related zinc finger transcription factor ATHB29. Plant Mol Biol. 2009;69:213–26.
pubmed: 18974936 doi: 10.1007/s11103-008-9419-0
Tehseen M, Cairns N, Sherson S, Cobbett CS. Metallochaperone-like genes in Arabidopsis thaliana. Metallomics. 2010;2:556–64.
pubmed: 21072340 doi: 10.1039/c003484c
Arnesano F, Banci L, Bertini I, Ciofi-baffoni S, Molteni E, Huffman DL, et al. Metallochaperones and metal-transporting ATPases: a comparative analysis of sequences and structures. Genome Res. 2002;12:255–71.
pubmed: 11827945 doi: 10.1101/gr.196802
Furukawa Y, Lim C, Tosha T, Yoshida K, Hagai T, Akiyama S et al. Identification of a novel zinc-binding protein, C1orf123, as an interactor with a heavy metal-associated domain. PLoS ONE. 2018;13.
Gao W, Xiao S, Li HY, Tsao SW, Chye ML. Arabidopsis thaliana acyl-CoA-binding protein ACBP2 interacts with heavy-metal-binding farnesylated protein AtFP6. New Phytol. 2009;181:89–102.
pubmed: 18823312 doi: 10.1111/j.1469-8137.2008.02631.x
Suzuki N, Yamaguchi Y, Koizumi N, Sano H. Functional characterization of a heavy metal binding protein CdI19 from Arabidopsis. Plant Journal: Cell Mol Biology. 2002;32:165–73.
doi: 10.1046/j.1365-313X.2002.01412.x
Jeon J, Kim J. Cold stress signaling networks in Arabidopsis. J Plant Biology. 2013;56:69–76.
doi: 10.1007/s12374-013-0903-y
Zhao YN, Wang MQ, Li C, Cao HW, Rono JK, Yang ZM. The metallochaperone OsHIPP56 gene is required for cadmium detoxification in rice crops. Environ Exp Bot. 2022;193.
Zhang X, Feng H, Feng C, Xu H, Huang X, Wang Q, et al. Isolation and characterisation of cDNA encoding a wheat heavy metal-associated isoprenylated protein involved in stress responses. Plant Biol. 2015;17:1176–86.
pubmed: 25951496 doi: 10.1111/plb.12344
Zschiesche W, Barth O, Daniel K, Boehme S, Rausche J, Humbeck K. The zinc-binding nuclear protein HIPP3 acts as an upstream regulator of the salicylate-dependent plant immunity pathway and of flowering time in Arabidopsis thaliana. New Phytol. 2015;207:1084–96.
pubmed: 25913773 doi: 10.1111/nph.13419
Tran LSP, Nakashima K, Sakuma Y, Osakabe Y, Qin F, Simpson SD, et al. Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances the expression of the ERD1 gene in Arabidopsis. Plant Journal: Cell Mol Biology. 2007;49:46–63.
doi: 10.1111/j.1365-313X.2006.02932.x
Chen G, Xiong S. OsHIPP24 is a copper metallochaperone which affects rice growth. J Plant Biology. 2021;64:145–53.
doi: 10.1007/s12374-020-09287-x
Guo T, Weber H, Niemann MCE, Theisl L, Leonte G, Novak O, et al. Arabidopsis HIPP proteins regulate endoplasmic reticulum-associated degradation of CIOX proteins and cytokinin responses. Mol Plant. 2021;14:1918–34.
pubmed: 34314894 doi: 10.1016/j.molp.2021.07.015
Tan DX, Manchester LC, Di MP, Martinez GR, Prado FM. Reiter RJ. Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation. Faseb J. 2007;21:1724–9.
pubmed: 17314136 doi: 10.1096/fj.06-7745com
Rugienius R, Šnipaitiene L, STanienė G, Šikšnianienė JB, Haimi P, Baniulis D, et al. Cold acclimation efficiency of different Prunus and Fragaria species and cultivars in vitro[J]. Zemdirbyste. 2016;103(2):207–14.
doi: 10.13080/z-a.2016.103.027
Gilmour SJ, Fowler SG, Thomashow MF. Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities [J]. Plant Mol Biol. 2004;54(5):767–81.
pubmed: 15356394 doi: 10.1023/B:PLAN.0000040902.06881.d4
Thomashow MF. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol. 2010;154:571–7.
pubmed: 20921187 pmcid: 2948992 doi: 10.1104/pp.110.161794
Song J, Guo B, Song F, Peng H, Yao Y, Zhang Y, et al. Genome-wide identification of gibberellins metabolic enzyme genes and expression profiling analysis during seed germination in maize [J]. Gene. 2011;482(1–2):34–42.
pubmed: 21640170 doi: 10.1016/j.gene.2011.05.008
Casson SA, Hetherington AM. Phytochrome B is required for light-mediated systemic control of stomatal development [J]. Curr Biol. 2014;24(11):1216–21.
pubmed: 24835461 pmcid: 4046225 doi: 10.1016/j.cub.2014.03.074
Turan MA, Elkarim AHA, Taban N, Taban S. Effect of salt stress on growth, stomatal resistance, proline and chlorophyll concentrations on maize plant [J]. Afr J Agric Res. 2009;4(9):893–7.
Van BF, Slooten L, Stassart JM, Moens T, Botterman J, Van MM, et al. Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize [J]. Plant Cell Physiol. 1999;40(5):515–23.
doi: 10.1093/oxfordjournals.pcp.a029572
Hou Q, Shen T, Yu R, Deng H, Wen X, Qiao G. Functional analysis of sweet cherry PavbHLH106 in the regulation of cold stress [J]. Plant Cell Rep. 2024;43(1).
Guo X, Liu D, Chong K. Cold signaling in plants: insights into mechanisms and regulation [J]. J Integr Plant Biol. 2018;60(9):745–56.
pubmed: 30094919 doi: 10.1111/jipb.12706
Shi Y, Ding Y, Yang S. Molecular reculation of CBF sicnalinc in colc acclimation [J]. Trends Plant Sci. 2018;23(7):623–37.
pubmed: 29735429 doi: 10.1016/j.tplants.2018.04.002
Rono JK, Sun D, Yang ZM, Metallochaperones. A critical regulator of metal homeostasis and beyond [J]. Gene. 2022;822.
Hala M, Zarsky V. Protein prenylation in plant stress responses [J]. Molecules. 2019;24(21).
Feller A, Machemer K, Braun EL, Grotewold E. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors [J]. Plant J. 2011;66(1):94–116.
pubmed: 21443626 doi: 10.1111/j.1365-313X.2010.04459.x
Chen BX, Peng YX, Yang XQ, Liu J. Delayed germination of Brassica parachinensis seeds by coumarin involves decreased GA
doi: 10.1017/S0960258521000167
Diaz-Vivancos P, Barba-Espin G, Antonio Hernandez J. Elucidating hormonal/ROS networks during seed germination: insights and perspectives [J]. Plant Cell Rep. 2013;32(10):1491–502.
pubmed: 23812175 doi: 10.1007/s00299-013-1473-7
Shu K, Liu XD, Xie Q, He ZH. Two faces of one seed: hormonal regulation of dormancy and germination [J]. Mol Plant. 2016;9(1):34–45.
pubmed: 26343970 doi: 10.1016/j.molp.2015.08.010
Tuan PA, Kumar R, Rehal PK, Toora PK, Ayele BT. Molecular mechanisms underlying abscisic acid/gibberellin balance in the control of seed dormancy and germination in cereals [J]. Front Plant Sci. 2018;9.
Ye N, Zhu G, Liu Y, Zhang A, Li Y, Liu R, et al. Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds [J]. J Exp Bot. 2012;63(5):1809–22.
pubmed: 22200664 doi: 10.1093/jxb/err336
Bailly C. The signaling role of ROS in the regulation of seed germination and dormancy [J]. Biochem J. 2019;476:3019–32.
pubmed: 31657442 doi: 10.1042/BCJ20190159
Zhou R, Yu X, Ottosen CO, Zhao T. High throughput sequencing of circRNAs in tomato leaves responding to multiple stresses of drought and heat [J]. Hortic Plant J. 2020;6(1):34–8.
doi: 10.1016/j.hpj.2019.12.004
Kollist H, Nuhkat M, Roelfsema MRG. Closing gaps: linking elements that control stomatal movement [J]. New Phytol. 2014;203(1):44–62.
pubmed: 24800691 doi: 10.1111/nph.12832
Haberman A, Ackerman M, Crane O, Kelner JJ, Costes E, Samach A. Different flowering response to various fruit loads in apple cultivars correlates with degree of transcript reaccumulation of a TFL1-encoding gene [J]. Plant J. 2016;87(2):161–73.
pubmed: 27121325 doi: 10.1111/tpj.13190
Li H, Gao W, Xue C, Zhang Y, Liu Z, Zhang Y, et al. Genome-wide analysis of the bHLH gene family in Chinese jujube (Ziziphus jujuba Mill.) and wild jujube [J]. BMC Genomics. 2019;20(1):568.
pubmed: 31291886 pmcid: 6617894 doi: 10.1186/s12864-019-5936-2
Guan Y, Hwarari D, Korboe HM, Ahmad B, Cao Y, Movahedi A et al. Low temperature stress-induced perception and molecular signaling pathways in plants [J]. Environ Exp Bot. 2023;207.
Han J, Li X, Li W, Yang Q, Li Z, Cheng Z, et al. Isolation and preliminary functional analysis of FvICE1, involved in cold and drought tolerance in Fragaria vesca through overexpression and CRISPR/Cas9 technologies [J]. Plant Physiol Bioch. 2023;196:270–80.
doi: 10.1016/j.plaphy.2023.01.048
Long H, Li Z, Suo H, Ou L, Miao W, Deng W. Study on the mechanism of grafting to improve the tolerance of pepper to low temperature [J]. Agronomy-Basel. 2023;13(5).
Luo P, Chen L, Chen Y, Shen Y, Cui Y. RmZAT10, a novel Cys2/His2 zinc finger transcription factor of Rosa multiflora, functions in cold tolerance through modulation of proline biosynthesis and ROS homeostasis [J]. Environ Exp Bot. 2022;198.
Rezayian M, Niknam V, Ebrahimzadeh H. Penconazole and calcium ameliorate drought stress in canola by upregulating the antioxidative enzymes [J]. Funct. Plant Biol. 2020;47(9):825–39.
Per TS, Khan NA, Reddy PS, Masood A, Hasanuzzaman M, Khan MIR, et al. Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics [J]. Plant Physiol Bioch. 2017;115:126–40.
doi: 10.1016/j.plaphy.2017.03.018
Jia Y, Ding Y, Shi Y, Zhang X, Gong Z, Yang S. The CBFs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis [J]. New Phytol. 2016;212(2):345–53.
pubmed: 27353960 doi: 10.1111/nph.14088
Shi Y, Huang J, Sun T, Wang X, Zhu C, Ai Y, Gu H. The precise regulation of different COR genes by individual CBF transcription factors in Arabidopsis thaliana [J]. J Integr Plant Biol. 2017;59(2):118–33.
pubmed: 28009483 doi: 10.1111/jipb.12515
Baid V. Low temperature and drought regulated gene expression in bermudagrass [J]. Turfgrass Environ Res Summ. 1994;1:32–3.
Wang S, Liang D, Li C, Hao Y, Ma F, Shu H. Influence of drought stress on the cellular ultrastructure and antioxidant system in leaves of drought-tolerant and drought-sensitive apple rootstocks [J]. Plant Physiol Bioch. 2012;51:81–9.
doi: 10.1016/j.plaphy.2011.10.014
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses [J]. Plant Cell Environ. 2010;33(4):453–67.
pubmed: 19712065 doi: 10.1111/j.1365-3040.2009.02041.x
Fang Y, Xiong L. General mechanisms of drought response and their application in drought resistance improvement in plants [J]. Cell Mol Life Sci. 2015;72(4):673–89.
pubmed: 25336153 doi: 10.1007/s00018-014-1767-0
Stockinger E, Gilmour S, Thomashow M. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit [J]. PNAS. 1997;94(3):1035–40.
pubmed: 9023378 pmcid: 19635 doi: 10.1073/pnas.94.3.1035
Shi Y, Ding Y, Yang S. Cold signal transduction and its interplay with phytohormones during cold acclimation [J]. Plant Cell Physiol. 2015;56(1):7–15.
pubmed: 25189343 doi: 10.1093/pcp/pcu115
Chinnusamy V, Ohta M, Kanrar S, Lee B, Hong X, Agarwal M, et al. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis[J]. Genes Dev. 2003;15(8):1043–54.
doi: 10.1101/gad.1077503
Agarwal M, Hao Y, Kapoor A, Dong C, Fujii H, Zheng X, et al. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance[J]. J Biol Chem. 2006;8(49):37636–45.
doi: 10.1074/jbc.M605895200
Zhao F, Li G, Hu P, Zhao X, Li L, Wei W et al. Identification of basic/helix-loop-helix transcription factors reveals candidate genes involved in anthocyanin biosynthesis from the strawberry white-flesh mutant [J]. Sci Rep. 2018;8.
Manara A, Fasani E, Molesini B, Dalcorso G, Pennisi F, Pandolfini T et al. The tomato metallocarboxypeptidase inhibitor I, which interacts with a heavy metal-associated isoprenylated protein, is implicated in plant response to cadmium [J]. Molecules. 2020;25(3).
Zheng Q, Yu Q, Wu N, Yao W, Li J, Lv K et al. A grape VvHOS1-interacting HIPP protein (VvHIPP21) negatively regulates cold and drought stress [J]. Environ Exp Bot. 2023;207.
Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, Olmstead RG et al. FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis [J]. PNAC. 2012;109(9): 3582-7.
Liu Y, Li X, Li K, Liu H, Lin C. Multiple bHLH proteins form heterodimers to mediate CRY2-dependent regulation of flowering-time in Arabidopsis [J]. PLoS Genet. 2013;9(10).
Cao X, Wen Z, Shen T, Cai X, Hou Q, Shang C et al. Overexpression of PavbHLH28 from Prunus avium enhances tolerance to cold stress in transgenic Arabidopsis [J]. BMC Plant Biol. 2023;23(1).
Shen T, Wen X, Wen Z, Qiu Z, Hou Q, Li Z et al. Genome-wide identification and expression analysis of bHLH transcription factor family in response to cold stress in sweet cherry (Prunus avium L.) [J]. Sci Hortic. 2021;279.
Sitakanta P, H X C, Ling Y. The interaction domains of the plant myc-like bHLH transcription factors can regulate the transactivation strength [J]. Planta. 2008;227(3).
Hou Q, Li S, Shang C, Wen Z, Cai X, Hong Y et al. Genome-wide characterization of chalcone synthase genes in sweet cherry and functional characterization of CpCHS1 under drought stress [J]. Front Plant Sci. 2022;13.
Cheng L, Zhang N, Huang B. Effects of 1-aminocyclopropane-1-carboxylate-deaminase–producing bacteria on perennial ryegrass growth and physiological responses to salinity stress[J]. J Am Soc Hortic Sci. 2016;141(3):233–41.
doi: 10.21273/JASHS.141.3.233
Liu Y, Liu Q, Li X, Zhang Z, Ai S, Liu C, et al. MdERF114 enhances the resistance of apple roots to Fusarium solani by regulating the transcription of MdPRX63[J]. Plant Physiol. 2023;192(3):2015–29.
pubmed: 36721923 pmcid: 10315273 doi: 10.1093/plphys/kiad057
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method [J]. Methods (San Diego, Calif). 2001;25(4): 402-8.

Auteurs

Runrun Yu (R)

Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences, Institute of Agro-bioengineering, Guizhou University, Guiyang, 550025, Guizhou Province, China.

Qiandong Hou (Q)

Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences, Institute of Agro-bioengineering, Guizhou University, Guiyang, 550025, Guizhou Province, China.

Hong Deng (H)

Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences, Institute of Agro-bioengineering, Guizhou University, Guiyang, 550025, Guizhou Province, China.

Ling Xiao (L)

Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences, Institute of Agro-bioengineering, Guizhou University, Guiyang, 550025, Guizhou Province, China.

Xiaowei Cai (X)

Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences, Institute of Agro-bioengineering, Guizhou University, Guiyang, 550025, Guizhou Province, China.

Chunqiong Shang (C)

Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences, Institute of Agro-bioengineering, Guizhou University, Guiyang, 550025, Guizhou Province, China.

Guang Qiao (G)

Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), College of Life Sciences, Institute of Agro-bioengineering, Guizhou University, Guiyang, 550025, Guizhou Province, China. gqiao@gzu.edu.cn.

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