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Comparative transcriptome analysis reveals the function of SlPRE2 in multiple phytohormones biosynthesis, signal transduction and stomatal development in tomato

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Abstract

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Transcriptomic, physiological, and qRT-PCR analysis revealed the potential mechanism by which SlPRE2 regulates plant growth and stomatal size via multiple phytohormone pathways in tomato.

Abstract

Paclobutrazol resistance proteins (PREs) are atypical members of the basic/helix-loop-helix (bHLH) transcription factor family that regulate plant morphology, cell size, pigment metabolism and abiotic stress in response to different phytohormones. However, little is known about the network regulatory mechanisms of PREs in plant growth and development in tomato. In this study, the function and mechanism of SlPRE2 in tomato plant growth and development were investigated. The quantitative RT-PCR results showed that the expression of SlPRE2 was regulated by multiple phytohormones and abiotic stresses. It showed light-repressed expression during the photoperiod. The RNA-seq results revealed that SlPRE2 regulated many genes involved in photosynthesis, chlorophyll metabolism, phytohormone metabolism and signaling, and carbohydrate metabolism, suggesting the role of SlPRE2 in gibberellin, brassinosteroid, auxin, cytokinin, abscisic acid and salicylic acid regulated plant development processes. Moreover, SlPRE2 overexpression plants showed widely opened stomata in young leaves, and four genes involved in stomatal development showed altered expression. Overall, the results demonstrated the mechanism by which SlPRE2 regulates phytohormone and stress responses and revealed the function of SlPRE2 in stomatal development in tomato. These findings provide useful clues for understanding the molecular mechanisms of SlPRE2-regulated plant growth and development in tomato.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

bHLH:

Basic/helix-loop-helix

TF:

Transcription factor

PREs:

Paclobutrazol resistances

PRE2OE:

SlPRE2 Overexpression lines

WT:

Wild-type

DEGs:

Differently expressed genes

GA3 :

Gibberellic acid

IAA:

Indoleacetic acid

MeJA:

Methyl jasmonate

ABA:

Abscisic acid

ACC:

1-Aminocyclopropane-1-carboxylic acid

BR:

Brassinosteroid

CK:

Cytokinin

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

References

  • Aamir M, Singh VK, Meena M, Upadhyay RS, Gupta VK, Singh S (2017) Structural and functional insights into WRKY3 and WRKY4 transcription factors to unravel the WRKY–DNA (W-Box) complex interaction in tomato (Solanum lycopersicum L.). A computational approach. Front Plant Sci 8:819

    Article  PubMed  PubMed Central  Google Scholar 

  • Ali AAM, Romdhane WB, Tarroum M, Al-Dakhil M, Al-Doss A, Alsadon AA, Hassairi A (2021) Analysis of salinity tolerance in tomato introgression lines based on morpho-physiological and molecular traits. Plants 10:2594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai M-Y, Fan M, Oh E, Wang Z-Y (2012) A triple helix-loop-helix/basic helix-loop-helix cascade controls cell elongation downstream of multiple hormonal and environmental signaling pathways in Arabidopsis. Plant Cell 24:4917–4929

    Article  PubMed  PubMed Central  Google Scholar 

  • Bharath P, Gahir S, Raghavendra AS (2021) Abscisic acid-induced stomatal closure: an important component of plant defense against abiotic and biotic stress. Front Plant Sci 12:615114

    Article  PubMed  PubMed Central  Google Scholar 

  • Castelain M, Le Hir R, Bellini C (2012) The non-DNA-binding bHLH transcription factor PRE3/bHLH135/ATBS1/TMO7 is involved in the regulation of light signaling pathway in Arabidopsis. Physiol Plantarum 145:450–460

    Article  CAS  Google Scholar 

  • Chen Y, Su D, Li J, Ying S, Deng H, He X, Zhu Y, Li Y, Chen Y, Pirrello J, Bouzayen M, Liu Y, Liu M (2020) Overexpression of bHLH95, a basic helix–loop–helix transcription factor family member, impacts trichome formation via regulating gibberellin biosynthesis in tomato. J Exp Bot 71:3450–3462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cirauqui C, Benito-Villalvilla C, Sánchez-Ramón S, Sirvent S, Diez-Rivero CM, Conejero L, Brandi P, Hernández-Cillero L, Ochoa JL, Pérez-Villamil B, Sancho D, Subiza JL, Palomares O (2018) Human dendritic cells activated with MV130 induce Th1, Th17 and IL-10 responses via RIPK2 and MyD88 signalling pathways. Eur J Immunol 48:180–193

    Article  CAS  PubMed  Google Scholar 

  • Du M, Zhao J, Tzeng DTW, Liu Y, Deng L, Yang T, Zhai Q, Wu F, Huang Z, Zhou M, Wang Q, Chen Q, Zhong S, Li C-B, Li C (2017) MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate-mediated plant immunity in tomato. Plant Cell 29:1883–1906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endo T, Fujii H, Sugiyama A, Nakano M, Nakajima N, Ikoma Y, Omura M, Shimada T (2016) Overexpression of a citrus basic helix-loop-helix transcription factor (CubHLH1), which is homologous to Arabidopsis activation-tagged bri1 suppressor 1 interacting factor genes, modulates carotenoid metabolism in transgenic tomato. Plant Sci 243:35–48

    Article  CAS  PubMed  Google Scholar 

  • Expósito-Rodríguez M, Borges AA, Borges-Pérez A, Pérez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8:131–131

    Article  PubMed  PubMed Central  Google Scholar 

  • Hao Y, Oh E, Choi G, Liang Z, Wang ZY (2012) Interactions between HLH and bHLH factors modulate light-regulated plant development. Mol Plant 5:688–697

    Article  PubMed  PubMed Central  Google Scholar 

  • Hao Y, Zong X, Ren P, Qian Y, Fu A (2021) Basic Helix-loop-helix (bHLH) transcription factors regulate a wide range of functions in Arabidopsis. Int J Mol Sci 22:7152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heang D, Sassa H (2012) Antagonistic actions of HLH/bHLH proteins are involved in grain length and weight in rice. PLoS ONE 7:e31325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong S-Y, Seo PJ, Ryu JY, Cho S-H, Woo J-C, Park C-M (2013) A competitive peptide inhibitor KIDARI negatively regulates HFR1 by forming nonfunctional heterodimers in Arabidopsis photomorphogenesis. Mol Cells 35:25–31

    Article  CAS  PubMed  Google Scholar 

  • Hornitschek P, Lorrain S, Zoete V, Michielin O, Fankhauser C (2009) Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28:3893–3902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Zhou J, Li Y, Quan R, Wang J, Huang R, Qin H (2021) Salt stress promotes abscisic acid accumulation to affect cell proliferation and expansion of primary roots in rice. Int J Mol Sci 22:10892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyun Y, Lee I (2006) KIDARI, Encoding a non-DNA binding bHLH protein, represses light signal transduction in Arabidopsis thaliana. Plant Mol Biol 61:283–296

    Article  CAS  PubMed  Google Scholar 

  • Ikeda M, Mitsuda N, Ohme-Takagi M (2013) ATBS1 INTERACTING FACTORs negatively regulate Arabidopsis cell elongation in the triantagonistic bHLH system. Plant Signal Behav 8:e23448

    Article  PubMed  PubMed Central  Google Scholar 

  • Job N, Datta S (2021) PIF3/HY5 module regulates BBX11 to suppress protochlorophyllide levels in dark and promote photomorphogenesis in light. New Phytol 230:190–204

    Article  CAS  PubMed  Google Scholar 

  • Jung C, Seo JS, Han SW, Koo YJ, Kim CH, Song SI, Nahm BH, Choi YD, Cheong JJ (2008) Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146:623–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keisham M, Mukherjee S, Bhatla SC (2018) Mechanisms of sodium transport in plants-progresses and challenges. Int J Mol Sci 19:647

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim T-W, Youn J-H, Park T-K, Kim E-J, Park C-H, Wang Z-Y, Kim S-K, Kim T-W (2018) RETRACTED: OST1 activation by the brassinosteroid-regulated kinase CDG1-LIKE1 in stomatal closure. Plant Cell 30:1848–1863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kravchik M, Shnaider Y, Abebie B, Shtarkman M, Kumari R, Kumar S, Leibman D, Spiegelman Z, Gal-On A (2022) Knockout of SlTOM1 and SlTOM3 results in differential resistance to tobamovirus in tomato. Mol Plant Pathol 23(9):1278–1289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Lee S, Yang K-Y, Kim Y-M, Park S-Y, Kim SY, Soh M-S (2006) Overexpression of PRE1 and its homologous genes activates gibberellin-dependent responses in Arabidopsis thaliana. Plant Cell Physiol 47:591–600

    Article  CAS  PubMed  Google Scholar 

  • Li S, Li X, Wei Z, Liu F (2020) ABA-mediated modulation of elevated CO2 on stomatal response to drought. Curr Opin Plant Biol 56:174–180

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Xu F, Chen Z, Teng Z, Sun K, Li X, Yu J, Zhang G, Liang Y, Huang X, Du L, Qian Y, Wang Y, Chu C, Tang J (2021) Synergistic interplay of ABA and BR signal in regulating plant growth and adaptation. Nat Plants 7:1108–1118

    Article  CAS  PubMed  Google Scholar 

  • Li J, Gong J, Zhang L, Shen H, Chen G, Xie Q, Hu Z (2022) Overexpression of SlPRE5, an atypical bHLH transcription factor, affects plant morphology and chlorophyll accumulation in tomato. J Plant Physiol 273:153698

    Article  CAS  PubMed  Google Scholar 

  • Li T, Shi Y, Zhu B, Zhang T, Feng Z, Wang X, Li X, You C (2022b) Genome-wide identification of apple atypical bHLH subfamily PRE members and functional characterization of MdPRE4.3 in response to abiotic stress. Front Genet 13:846559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livne S, Lor VS, Nir I, Eliaz N, Aharoni A, Olszewski NE, Eshed Y, Weiss D (2015) Uncovering DELLA-independent gibberellin responses by characterizing new tomato procera mutants. Plant Cell 27:1579–1594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Vidriero I, Godoy M, Grau J, Peñuelas M, Solano R, Franco-Zorrilla JM (2021) DNA features beyond the transcription factor binding site specify target recognition by plant MYC2-related bHLH proteins. Plant Commun 2(6):100232

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu J, He J, Zhou X, Zhong J, Li J, Liang Y-K (2019) Homologous genes of epidermal patterning factor regulate stomatal development in rice. J Plant Physiol 234–235:18–27

    Article  PubMed  Google Scholar 

  • Mahadevan C, Krishnan A, Saraswathy GG, Surendran A, Jaleel A, Sakuntala M (2016) Transcriptome- assisted label-free quantitative proteomics analysis reveals novel insights into Piper nigrum-phytophthora capsici phytopathosystem. Front Plant Sci 7:785

    Article  PubMed  PubMed Central  Google Scholar 

  • Medina-Puche L, Martínez-Rivas FJ, Molina-Hidalgo FJ, Mercado JA, Moyano E, Rodríguez-Franco A, Caballero JL, Muñoz-Blanco J, Blanco-Portales R (2019) An atypical HLH transcriptional regulator plays a novel and important role in strawberry ripened receptacle. BMC Plant Biol 19:586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina-Puche L, Martínez-Rivas FJ, Molina-Hidalgo FJ, García-Gago JA, Mercado JA, Caballero JL, Muñoz-Blanco J, Blanco-Portales R (2021) Ectopic expression of the atypical HLH FaPRE1 gene determines changes in cell size and morphology. Plant Sci 305:110830

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970

    Article  CAS  PubMed  Google Scholar 

  • Nir I, Shohat H, Panizel I, Olszewski N, Aharoni A, Weiss D (2017) The tomato DELLA protein PROCERA acts in guard cells to promote stomatal closure. Plant Cell 29:3186–3197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niwa T, Kondo T, Nishizawa M, Kajita R, Kakimoto T, Ishiguro S (2013) EPIDERMAL PATTERNING FACTOR LIKE5 peptide represses stomatal development by inhibiting meristemoid maintenance in Arabidopsis thaliana. Biosci Biotechnol Biochem 77:1287–1295

    Article  CAS  PubMed  Google Scholar 

  • Oh JE, Kwon Y, Kim JH, Noh H, Hong S-W, Lee H (2011) A dual role for MYB60 in stomatal regulation and root growth of Arabidopsis thaliana under drought stress. Plant Mol Biol 77:91–103

    Article  CAS  PubMed  Google Scholar 

  • Pan Y, Seymour GB, Lu C, Hu Z, Chen X, Chen G (2012) An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep 31:349–360

    Article  CAS  PubMed  Google Scholar 

  • Qian Y, Zhang T, Yu Y, Gou L, Yang J, Xu J, Pi E (2021) Regulatory mechanisms of bHLH transcription factors in plant adaptive responses to various abiotic stresses. Front Plant Sci 12:677611

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiu Y, Tao R, Feng Y, Xiao Z, Zhang D, Peng Y, Wen X, Wang Y, Guo H (2021) EIN3 and RSL4 interfere with an MYB-bHLH-WD40 complex to mediate ethylene-induced ectopic root hair formation in Arabidopsis. Proc Natl Acad Sci USA 118:e2110004118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosado D, Gramegna G, Cruz A, Lira BS, Freschi L, de Setta N, Rossi M (2016) Phytochrome Interacting Factors (PIFs) in Solanum lycopersicum: diversity, evolutionary history and expression profiling during different developmental processes. PLoS ONE 11:e0165929

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanagi M, Aoyama S, Kubo A, Lu Y, Sato Y, Ito S, Abe M, Mitsuda N, Ohme-Takagi M, Kiba T, Nakagami H, Rolland F, Yamaguchi J, Imaizumi T, Sato T (2021) Low nitrogen conditions accelerate flowering by modulating the phosphorylation state of FLOWERING BHLH 4 in Arabidopsis. Proc Natl Acad Sci USA 118:e2022942118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo PJ, Hong S-Y, Kim S-G, Park C-M (2011) Competitive inhibition of transcription factors by small interfering peptides. Trends Plant Sci 16:541–549

    Article  CAS  PubMed  Google Scholar 

  • Shin K, Lee I, Kim E, Park SK, Soh M-S, Lee S (2019) PACLOBUTRAZOL-RESISTANCE gene family regulates floral organ growth with unequal genetic redundancy in Arabidopsis thaliana. Int J Mol Sci 20:869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15:1749–1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trigg SA, Garza RM, MacWilliams A, Nery JR, Bartlett A, Castanon R, Goubil A, Feeney J, O’Malley R, S-sC H, Zhang ZZ, Galli M, Ecker JR (2017) CrY2H-seq: a massively multiplexed assay for deep-coverage interactome mapping. Nat Methods 14:819–825

    Article  CAS  Google Scholar 

  • Verma D, Jalmi SK, Bhagat PK, Verma N, Sinha AK (2020) A bHLH transcription factor, MYC2, imparts salt intolerance by regulating proline biosynthesis in Arabidopsis. FEBS J 287:2560–2576

    Article  CAS  PubMed  Google Scholar 

  • Vonapartis E, Mohamed D, Li J, Pan W, Wu J, Gazzarrini S (2022) CBF4/DREB1D represses XERICO to attenuate ABA, osmotic and drought stress responses in Arabidopsis. Plant J 110:961–977

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Zhu Y, Fujioka S, Asami T, Li J, Li J (2009) Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix-loop-helix proteins. Plant Cell 21:3781–3791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Zhu Z (2021) PIF4 and PIF4-interacting proteins: at the nexus of plant light, temperature and hormone signal integrations. Int J Mol Sci 22:10304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang C, Huang S, Zeng Y, Liu C, Ma Q, Pruneda-Paz J, Kay SA, Li L (2021) Two bHLH transcription factors, bHLH48 and bHLH60, associate with phytochrome interacting factor 7 to regulate hypocotyl elongation in Arabidopsis. Cell Rep 35(5):109054

    Article  CAS  PubMed  Google Scholar 

  • Zhang L-Y, Bai M-Y, Wu J, Zhu J-Y, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Sun X, Yang H, Xu Y, Kim S-H, Fujioka S, Lin W-H, Chong K, Lu T, Wang Z-Y (2009) Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21:3767–3780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Bai M-y, Chong K (2014) Brassinosteroid-mediated regulation of agronomic traits in rice. Plant Cell Rep 33:683–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Kang J, Xie Q, Gong J, Shen H, Chen Y, Chen G, Hu Z (2020) The basic helix-loop-helix transcription factor bHLH95 affects fruit ripening and multiple metabolisms in tomato. J Exp Bot 71:6311–6327

    Article  CAS  PubMed  Google Scholar 

  • Zheng K, Wang Y, Zhang N, Jia Q, Wang X, Hou C, Chen J-G, Wang S (2017) Involvement of PACLOBUTRAZOL RESISTANCE6/KIDARI, an atypical bHLH transcription factor, in auxin responses in Arabidopsis. Front Plant Sci 8:1813

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng K, Wang Y, Wang S (2019) The non-DNA binding bHLH transcription factor paclobutrazol resistances are involved in the regulation of ABA and salt responses in Arabidopsis. Plant Physiol Biochem 139:239–245

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, Chen G, Guo X, Yin W, Yu X, Hu J, Hu Z (2017) Overexpression of SlPRE2, an atypical bHLH transcription factor, affects plant morphology and fruit pigment accumulation in tomato. Sci Rep-UK 7:5786

    Article  Google Scholar 

  • Zhu Z, Liang H, Chen G, Li F, Wang Y, Liao C, Hu Z (2019) The bHLH transcription factor SlPRE2 regulates tomato fruit development and modulates plant response to gibberellin. Plant Cell Rep 38:1053–1064

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 32160711 and 31960605) and the Natural Science Foundation of Jiangxi Province (Grant No. 20202BABL215009).

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Authors and Affiliations

  1. Institute of Jiangxi Oil-Tea Camellia, Jiujiang University, Jiujiang, 332000, Jiangxi, China

    Zhiguo Zhu, Menglin Luo, Jialing Li, Zixin Liu, Dapeng Fu, Huiwen Zhou & Anpei Zhou

  2. College of Pharmacy and Life Sciences, Jiujiang University, Jiujiang, 332000, Jiangxi, China

    Zhiguo Zhu, Menglin Luo, Jialing Li, Zixin Liu & Dapeng Fu

  3. College of Biological Science and Agriculture, Qiannan Normal University for Nationalities, Duyun, 558000, Guizhou, China

    Baolu Cui

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  1. Zhiguo Zhu
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Contributions

ZZ and ML conceived the study and designed the experiments. ZZ, ML, JL, ZL and DF performed the experiments. ZZ and HZ analyzed the data. ZZ, BC and AZ drafted the manuscript. All the authors participated in the revision of the manuscript.

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Correspondence to Zhiguo Zhu.

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Zhu, Z., Luo, M., Li, J. et al. Comparative transcriptome analysis reveals the function of SlPRE2 in multiple phytohormones biosynthesis, signal transduction and stomatal development in tomato. Plant Cell Rep 42, 921–937 (2023). https://doi.org/10.1007/s00299-023-03001-0

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