Abstract
Main conclusion
Overexpression of MdLBD3 in Arabidopsis reduced sensitivity to salt and drought stresses and was instrumental in promoting early flowering.
Abstract
Salt and drought stresses have serious effects on plant growth. LATERAL ORGAN BOUNDARY DOMAIN (LBD) proteins are a plant-specific transcription factors (TFs) family and play important roles in plants in resisting to abiotic stress. However, about the function of LBDs in apple and other woody plants is little known. In this study, protein sequences of the LBD family TFs in apples were identified which contained conserved LOB domains. The qRT-PCR analysis showed that the MdLBD3 gene was widely expressed in various tissues and organs. The subcellular localization assay showed that the MdLBD3 protein was localized in the nucleus. Ectopic expression of MdLBD3 in Arabidopsis positively regulated its salt and drought resistance, and promoted early flowering. Collectively, these results showed that MdLBD3 improved the abiotic stress resistance, plant growth and development. Overall, this study provided a new gene for breeding that can increase the abiotic stress tolerance in apple.
Similar content being viewed by others
Data availability
The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- LBD:
-
LATERAL ORGAN BOUNDARIES (LOB) DOMAIN
- TF:
-
Transcription factor
References
An JP, Qu FJ, Yao JF, Wang XN, You CX, Wang XF, Hao YJ (2017) The bZIP transcription factor MdHY5 regulates anthocyanin accumulation and nitrate assimilation in apple. Hortic Res 4:17023
An JP, Li R, Qu FJ, You CX, Wang XF, Hao YJ (2018) An apple NAC transcription factor negatively regulates cold tolerance via CBF-dependent pathway. J Plant Physiol 221:74–80
An JP, Zhang XW, Bi SQ, You CX, Wang XF, Hao YJ (2020) The ERF transcription factor MdERF38 promotes drought stress-induced anthocyanin biosynthesis in apple. Plant J 101(3):573–589
Chen XD, Wang J, Zhao MZ, Yuan HZ (2017) Identification and expression analysis of LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factor genes in Fragaria vesca. Can J Plant Sci 98(2):288–299
Chen K, Song M, Guo Y, Liu L, Xue H, Dai H, Zhang Z (2019) MdMYB46 could enhance salt and osmotic stress tolerance in apple by directly activating stress-responsive signals. Plant Biotechnol J 17(12):2341–2355
Chong L, Xu R, Huang P, Guo P, Zhu M, Du H, Sun X, Ku L, Zhu JK, Zhu Y (2022) The tomato OST1-VOZ1 module regulates drought-mediated flowering. Plant Cell 34(5):2001–2018
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743
Danquah A, de Zelicourt A, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32(1):40–52
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379
Dietz KJ, Zörb C, Geilfus CM (2021) Drought and crop yield. Plant Biol 23(6):881–893
Dong Q, Zheng W, Duan D, Huang D, Wang Q, Liu C, Li C, Gong X, Li C, Mao K, Ma F (2020) MdWRKY30, a group IIa WRKY gene from apple, confers tolerance to salinity and osmotic stresses in transgenic apple callus and Arabidopsis seedlings. Plant Sci 299:110611
Fan M, Xu C, Xu K, Hu Y (2012) LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res 22(7):1169–1180
Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31(6):713–727
Freytes SN, Canelo M, Cerdán PD (2021) Regulation of flowering time: When and where? Curr Opin Plant Biol 63:102049
Grabska J, Beć K, Ueno N, Huck C (2023) Analyzing the quality parameters of apples by spectroscopy from Vis/NIR to NIR region: a comprehensive review. Foods 12(10):1946
Guan C, Wu B, Ma S, Zhang J, Liu X, Wang H, Zhang J, Gao R, Jiang H, Jia C (2023) Genome-wide characterization of LBD transcription factors in switchgrass (Panicum virgatum L.) and the involvement of PvLBD12 in salt tolerance. Plant Cell Rep 42(4):735–748
Hu W, Huang C, Deng X, Zhou S, Chen L, Li Y, Wang C, Ma Z, Yuan Q, Wang Y, Cai R, Liang X, Yang G, He G (2013) TaASR1, a transcription factor gene in wheat, confers drought stress tolerance in transgenic tobacco. Plant Cell Environ 36(8):1449–1464
Hu DG, Yu JQ, Han PL, Xie XB, Sun CH, Zhang QY, Wang JH, Hao YJ (2019) The regulatory module MdPUB29-MdbHLH3 connects ethylene biosynthesis with fruit quality in apple. New Phytol 221(4):1966–1982
Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43(5):467–478
Jia R, Li C, Wang Y, Qin X, Meng L, Sun X (2022) Genome-wide analysis of LBD transcription factor genes in Dendrobium catenatum. Int J Mol Sci 23(4):2089
Jiao P, Wei X, Jiang Z, Liu S, Guan S, Ma Y (2022) ZmLBD2 a maize (Zea mays L.) lateral organ boundaries domain (LBD) transcription factor enhances drought tolerance in transgenic Arabidopsis thaliana. Front Plant Sci 13:1000149
Kim MJ, Kim M, Lee MR, Park SK, Kim J (2015) LATERAL ORGAN BOUNDARIES DOMAIN (LBD)10 interacts with SIDECAR POLLEN/LBD27 to control pollen development in Arabidopsis. Plant J 81(5):794–809
Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40(D1):D1202–D1210
Latchman DS (1997) Transcription factors: an overview. Int J Biochem Cell Biol 29(12):1312
Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43(1):47–56
Liu L, Zhang J, Xu J, Li Y, Guo L, Wang Z, Zhang X, Zhao B, Guo YD, Zhang N (2020) CRISPR/Cas9 targeted mutagenesis of SlLBD40, a lateral organ boundaries domain transcription factor, enhances drought tolerance in tomato. Plant Sci 301:110683
Liu HF, Zhang TT, Liu YQ, Kang H, Rui L, Wang DR, You CX, Xue XM, Wang XF (2023) Genome-wide analysis of the 6B-INTERACTING PROTEIN1 gene family with functional characterization of MdSIP1-2 in Malus domestica. Plant Physiol Biochem 195:89–100
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408
Majer C, Hochholdinger F (2011) Defining the boundaries: structure and function of LOB domain proteins. Trends Plant Sci 16(1):47–52
Majer C, Xu C, Berendzen KW, Hochholdinger F (2012) Molecular interactions of ROOTLESS CONCERNING CROWN AND SEMINAL ROOTS, a LOB domain protein regulating shoot-borne root initiation in maize (Zea mays L.). Philos Trans R Soc Lond B Biol Sci 367(1595):1542–1551
Matsumura Y, Iwakawa H, Machida Y, Machida C (2009) Characterization of genes in the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) family in Arabidopsis thaliana, and functional and molecular comparisons between AS2 and other family members. Plant J 58(3):525–537
Pan J, Zhang M, Kong X, Xing X, Liu Y, Zhou Y, Liu Y, Sun L, Li D (2012) ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta 235(4):661–676
Park HJ, Kim WY, Pardo JM, Yun DJ (2016) Molecular interactions between flowering time and abiotic stress pathways. Int Rev Cell Mol Biol 327:371–412
Ren YR, Yang YY, Zhang R, You CX, Zhao Q, Hao YJ (2019) MdGRF11, an apple 14-3-3 protein, acts as a positive regulator of drought and salt tolerance. Plant Sci 288:110219
Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21(11):3567–3584
Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y (2001) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128(10):1771–1783
Shinozaki KY-SK (1994) A nove1 cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low temperature, or high-salt stress. Plant Cell 6(2):251–264
Shuai B, Reynaga-Peña CG, Springer PS (2019) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol 129(2):747–761
Spoel SH, van Ooijen G (2014) Circadian redox signaling in plant immunity and abiotic stress. Antioxid Redox Signal 20(18):3024–3039
Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16(2):123–132
Waadt R, Seller CA, Hsu PK, Takahashi Y, Munemasa S, Schroeder JI (2022) Plant hormone regulation of abiotic stress responses. Nat Rev Mol Cell Biol 23(10):680–694
Wang X, Zhang S, Su L, Liu X, Hao Y (2013) A genome-wide analysis of the LBD (LATERAL ORGAN BOUNDARIES domain) gene family in Malus domestica with a functional characterization of MdLBD11. PLoS ONE 8(2):e57044
Wang J, Zhang W, Cheng Y, Feng L (2021) Genome-wide identification of LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors and screening of salt stress candidates of Rosa rugosa Thunb. Biology 10(10):992
Wang DR, Yang K, Wang X, You CX (2022) A C2H2-type zinc finger transcription factor, MdZAT17, acts as a positive regulator in response to salt stress. J Plant Physiol 275:153737
Wu M, He W, Wang L, Zhang X, Wang K, Xiang Y (2023) PheLBD29, an LBD transcription factor from Moso bamboo, causes leaf curvature and enhances tolerance to drought stress in transgenic Arabidopsis. J Plant Physiol 280:153865
Wu X, Wang Z, Du A, Gao H, Liang J, Yu W, Yu H, Fan S, Chen Q, Guo J, Xiao Y, Peng F (2024) Transcription factor LBD16 targets cell wall modification/ion transport genes in peach lateral root formation. Plant Physiol. https://doi.org/10.1093/plphys/kiae017
Xia Y, Chen F, Du Y, Liu C, Bu G, Xin Y, Liu B (2019) A modified SDS-based DNA extraction method from raw soybean. Biosci Rep 39(2):BSR20182271
Yang Y, Guo Y (2018) Unraveling salt stress signaling in plants. J Integr Plant Biol 60(9):796–804
Ye L, Wang X, Lyu M, Siligato R, Eswaran G, Vainio L, Blomster T, Zhang J, Mähönen AP (2021) Cytokinins initiate secondary growth in the Arabidopsis root through a set of LBD genes. Curr Biol 31(15):3365-3373.e7
Yu J, Xie Q, Li C, Dong Y, Zhu S, Chen J (2020) Comprehensive characterization and gene expression patterns of LBD gene family in Gossypium. Planta 251:81
Zhang H, Sun X, Dai M (2022) Improving crop drought resistance with plant growth regulators and rhizobacteria: mechanisms, applications, and perspectives. Plant Commun 3(1):100228
Zhao D, Chen P, Chen Z, Zhang L, Wang Y, Xu L (2023) Genome-wide analysis of the LBD family in rice: gene functions, structure and evolution. Comput Biol Med 153:106452
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Funding
This work was supported by the National Natural Science Foundation of China (32272683), the Shandong Province Key R&D Program of China (2022TZXD008-02), and the China Agriculture Research System of MOF and MARA (CARS-27).
Author information
Authors and Affiliations
Contributions
YL: conducted experiments and wrote original draft. XHA, HL, and TZ: designed experiments. XL, RL, CL, and YT: collated data. CY and XFW: revised the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, Y., An, XH., Liu, H. et al. Cloning and functional identification of apple LATERAL ORGAN BOUNDARY DOMAIN 3 (LBD3) transcription factor in the regulation of drought and salt stress. Planta 259, 125 (2024). https://doi.org/10.1007/s00425-024-04373-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-024-04373-7