Skip to main content
SpringerLink
Log in

AsHSP26.2, a creeping bentgrass chloroplast small heat shock protein positively regulates plant development

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

The creeping bentgrass small heat shock protein AsHSP26.2 positively regulates plant growth and is a novel candidate for use in crop genetic engineering for enhanced biomass production and grain yield.

Abstract

Small heat shock proteins (sHSPs), a family of proteins with high level of diversity, significantly influence plant stress tolerance and plant development. We have cloned a creeping bentgrass chloroplast-localized sHSP gene, AsHSP26.2 responsive to IAA, GA and 6-BA stimulation. Transgenic creeping bentgrass overexpressing AsHSP26.2 exhibited significantly enhanced plant growth with increased stolon number and length as well as enlarged leaf blade width and leaf sheath diameters, but inhibited leaf trichomes initiation and development in the abaxial epidermis. These phenotypes are completely opposite to those displayed in the transgenic plants overexpressing AsHSP26.8, another chloroplast sHSP26 isoform that contains additional seven amino acids (AEGQGDG) between the consensus regions III and IV (Sun et al., Plant Cell Environ 44:1769–1787, 2021). Furthermore, AsHSP26.2 overexpression altered phytohormone biosynthesis and signaling transduction, resulting in elevated auxin and gibberellins (GA) accumulation. The results obtained provide novel insights implicating the sHSPs in plant growth and development regulation, and strongly suggest AsHSP26.2 to be a novel candidate for use in crop genetic engineering for enhanced plant biomass production and grain yield.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) repository (BioProject ID: PRJNA865009).

References

  • Banerjee A, Roychoudhury A (2018) Small heat shock proteins: structural assembly and functional responses against heat stress in plants. Plant Metabolites and Regulation Under Environmental Stress 367–376

  • Bart R, Chern M, Park CJ, Bartley L, Ronald PC (2006) A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods 2:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Beauchet A, Gevaudant F, Gonzalez N, Chevalier C (2021) In search of the still unknown function of FW2.2/CELL NUMBER REGULATOR, a major regulator of fruit size in tomato. J Exp Bot 72:5300–5311

    Article  PubMed  CAS  Google Scholar 

  • Binenbaum J, Weinstain R, Shani E (2018) Gibberellin localization and transport in plants. Trends Plant Sci 23:410–421

    Article  PubMed  CAS  Google Scholar 

  • Blazquez MA, Nelson DC, Weijers D (2020) Evolution of plant hormone response pathways. Annu Rev Plant Biol 71:327–353

    Article  PubMed  CAS  Google Scholar 

  • Bomer M, Perez-Salamo I, Florance HV, Salmon D, Dudenhoffer JH, Finch P, Cinar A, Smirnoff N, Harvey A, Devoto A (2021) Jasmonates induce Arabidopsis bioactivities selectively inhibiting the growth of breast cancer cells through CDC6 and mTOR. New Phytol 229:2120–2134

    Article  PubMed  Google Scholar 

  • Cance C, Martin-Arevalillo R, Boubekeur K, Dumas R (2022) Auxin response factors are keys to the many auxin doors. New Phytol 235:402–419

    Article  PubMed  Google Scholar 

  • Claeys H, De Bodt S, Inze D (2014) Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends Plant Sci 19:231–239

    Article  PubMed  CAS  Google Scholar 

  • Das S, Weijers D, Borst JW (2021) Auxin response by the numbers. Trends Plant Sci 26:442–451

    Article  PubMed  CAS  Google Scholar 

  • Daviere JM, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151

    Article  PubMed  CAS  Google Scholar 

  • Debernardi JM, Mecchia MA, Vercruyssen L, Smaczniak C, Kaufmann K, Inze D, Rodriguez RE, Palatnik JF (2014) Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity. Plant J 79:413–426

    Article  PubMed  CAS  Google Scholar 

  • Escobar MR, Feussner I, Valle EM (2021) Mitochondrial small heat shock proteins are essential for normal growth of Arabidopsis thaliana. Front Plant Sci 12:600426

    Article  PubMed  PubMed Central  Google Scholar 

  • Fung-Uceda J, Lee K, Seo PJ, Polyn S, De Veylder L, Mas P (2018) The circadian clock sets the time of DNA replication licensing to regulate growth in Arabidopsis. Dev Cell 45(101–113):e104

    Google Scholar 

  • Gao S, Chu C (2020) Gibberellin metabolism and signaling: targets for improving agronomic performance of crops. Plant Cell Physiol 61:1902–1911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo M, Rupe MA, Dieter JA, Zou JJ, Spielbauer D, Duncan KE, Howard RJ, Hou ZL, Simmons CR (2010) Cell number regulator1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell 22:1057–1073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han G, Li Y, Yang Z, Wang C, Zhang Y, Wang B (2022) Molecular mechanisms of plant trichome development. Front Plant Sci 13:910228

    Article  PubMed  PubMed Central  Google Scholar 

  • Inthima P, Nakano M, Otani M, Niki T, Nishijima T, Koshioka M, Supaibulwatana K (2017) Overexpression of the gibberellin 20-oxidase gene from Torenia fournieri resulted in modified trichome formation and terpenoid of metabolites Artemisia annua L. (vol 129, pg 223, 2017). Plant Cell Tiss Org 130:689–689

    Article  Google Scholar 

  • Jacob P, Hirt H, Bendahmane A (2017) The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J 15:405–414

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jha P, Ochatt SJ, Kumar V (2020) WUSCHEL: a master regulator in plant growth signaling. Plant Cell Rep 39:431–444

    Article  PubMed  CAS  Google Scholar 

  • Kaur H, Petla BP, Kamble NU, Singh A, Rao V, Salvi P, Ghosh S, Majee M (2015) Differentially expressed seed aging responsive heat shock protein OsHSP18.2 implicates in seed vigor, longevity and improves germination and seedling establishment under abiotic stress. Front Plant Sci 6:713

    Article  PubMed  PubMed Central  Google Scholar 

  • Kieber JJ, Schaller GE (2018) Cytokinin signaling in plant development. Development 145(4):dev149344

    Article  PubMed  Google Scholar 

  • Kim JH, Kende H (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci USA 101:13374–13379

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD (2007a) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    Article  PubMed  CAS  Google Scholar 

  • Kotak S, Vierling E, Baumlein H, von Koskull-Doring P (2007b) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19:182–195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lavy M, Estelle M (2016) Mechanisms of auxin signaling. Development 143:3226–3229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leyser O (2018) Auxin signaling. Plant Physiol 176:465–479

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Yan J, Wang K, Li D, Yang R, Luo H, Zhang W (2021) MiR396-GRF module associates with switchgrass biomass yield and feedstock quality. Plant Biotechnol J 19:1523–1536

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    Article  PubMed  PubMed Central  Google Scholar 

  • Lubaretz O, Zur Nieden U (2002) Accumulation of plant small heat-stress proteins in storage organs. Planta 215:220–228

    Article  PubMed  CAS  Google Scholar 

  • Luo H, Hu Q, Nelson K, Longo C, Kausch AP, Chandlee JM, Wipff JK, Fricker CR (2004) Agrobacterium tumefaciens-mediated creeping bentgrass (Agrostis stolonifera L.) transformation using phosphinothricin selection results in a high frequency of single-copy transgene integration. Plant Cell Rep 22:645–652

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Guan X, Li J, Pan R, Wang L, Liu F, Ma H, Zhu S, Hu J, Ruan YL, Chen X, Zhang T (2019) Mitochondrial small heat shock protein mediates seed germination via thermal sensing. Proc Natl Acad Sci USA 116:4716–4721

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  • Mazzoni-Putman SM, Brumos J, Zhao C, Alonso JM, Stepanova AN (2021a) Auxin interactions with other hormones in plant development. Cold Spring Harb Perspect Biol 13:a039990

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mazzoni-Putman SM, Brumos J, Zhao CS, Alonso JM, Stepanova AN (2021b) Auxin interactions with other hormones in plant development. Cold Spring Harb Perspect Biol 13:a03990

    Article  Google Scholar 

  • Mu C, Wang S, Zhang S, Pan J, Chen N, Li X, Wang Z, Liu H (2011) Small heat shock protein LimHSP16.45 protects pollen mother cells and tapetal cells against extreme temperatures during late zygotene to pachytene stages of meiotic prophase I in David Lily. Plant Cell Rep 30:1981–1989

    Article  PubMed  CAS  Google Scholar 

  • Noir S, Bomer M, Takahashi N, Ishida T, Tsui TL, Balbi V, Shanahan H, Sugimoto K, Devoto A (2013) Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol 161:1930–1951

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Omidbakhshfard MA, Proost S, Fujikura U, Mueller-Roeber B (2015) Growth-regulating factors (GRFs): a small transcription factor family with important functions in plant biology. Mol Plant 8:998–1010

    Article  PubMed  CAS  Google Scholar 

  • Perez DE, Hoyer JS, Johnson AI, Moody ZR, Lopez J, Kaplinsky NJ (2009) BOBBER1 is a noncanonical Arabidopsis small heat shock protein required for both development and thermotolerance. Plant Physiol 151:241–252

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reddy PS, Kavi Kishor PB, Seiler C, Kuhlmann M, Eschen-Lippold L, Lee J, Reddy MK, Sreenivasulu N (2014) Unraveling regulation of the small heat shock proteins by the heat shock factor HvHsfB2c in barley: its implications in drought stress response and seed development. PLoS One 9:e89125

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819:104–119

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Sun C, Li Z, Hu Q, Han L, Luo H (2016) AsHSP17, a creeping bentgrass small heat shock protein modulates plant photosynthesis and ABA-dependent and independent signalling to attenuate plant response to abiotic stress. Plant Cell Environ 39:1320–1337

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Zhu J, Li X, Li Z, Han L, Luo H (2020) AsHSP26.8a, a creeping bentgrass small heat shock protein integrates different signaling pathways to modulate plant abiotic stress response. BMC Plant Biol 20:184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun X, Huang N, Li X, Zhu J, Bian X, Li H, Wang L, Hu Q, Luo H (2021) A chloroplast heat shock protein modulates growth and abiotic stress response in creeping bentgrass. Plant Cell Environ 44:1769–1787

    Article  PubMed  CAS  Google Scholar 

  • Ul Haq S, Khan A, Ali M, Khattak AM, Gai WX, Zhang HX, Wei AM, Gong ZH (2019) Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. Int J Mol Sci 20:5321

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Volkov RA, Panchuk II, Schoffl F (2005) Small heat shock proteins are differentially regulated during pollen development and following heat stress in tobacco. Plant Mol Biol 57:487–502

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Luthe DS (2003) Heat sensitivity in a bentgrass variant. Failure to accumulate a chloroplast heat shock protein isoform implicated in heat tolerance. Plant Physiol 133:319–327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Z, Yang Z, Li F (2019) Updates on molecular mechanisms in the development of branched trichome in Arabidopsis and nonbranched in cotton. Plant Biotechnol J 17:1706–1722

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Y, Zhou Q, Meng Z, Abid MA, Wang Y, Wei Y, Guo S, Zhang R, Liang C (2022) Multi-dimensional molecular regulation of trichome development in Arabidopsis and cotton. Front Plant Sci 13:892381

    Article  PubMed  PubMed Central  Google Scholar 

  • Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64:391–403

    Article  PubMed  CAS  Google Scholar 

  • Waters ER, Vierling E (2020) Plant small heat shock proteins—evolutionary and functional diversity. New Phytol 227:24–37

    Article  PubMed  CAS  Google Scholar 

  • Wu X, Gong F, Yang L, Hu X, Tai F, Wang W (2014) Proteomic analysis reveals differential accumulation of small heat shock proteins and late embryogenesis abundant proteins between ABA-deficient mutant vp5 seeds and wild-type Vp5 seeds in maize. Front Plant Sci 5:801

    PubMed  Google Scholar 

  • Wu J, Gao T, Hu J, Zhao L, Yu C, Ma F (2022) Research advances in function and regulation mechanisms of plant small heat shock proteins (sHSPs) under environmental stresses. Sci Total Environ 825:154054

    Article  ADS  PubMed  CAS  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

    Article  PubMed  CAS  Google Scholar 

  • Yang G, Wang Y, Zhang K, Gao C (2014) Expression analysis of nine small heat shock protein genes from Tamarix hispida in response to different abiotic stresses and abscisic acid treatment. Mol Biol Rep 41:1279–1289

    Article  PubMed  CAS  Google Scholar 

  • Yang R, Wu Z, Bai C, Sun Z, Wang M, Huo Y, Zhang H, Wang Y, Zhou H, Dai S, Liu W, Fu C (2021) Overexpression of PvWOX3a in switchgrass promotes stem development and increases plant height. Hortic Res 8:252

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang Z, Du H, Sun J, Xing X, Kong Y, Li W, Li X, Zhang C (2022a) A nodule-localized small heat shock protein GmHSP17.1 confers nodule development and nitrogen fixation in soybean. Front Plant Sci 13:838718

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Du H, Xing X, Li W, Kong Y, Li X, Zhang C (2022b) A small heat shock protein, GmHSP17.9, from nodule confers symbiotic nitrogen fixation and seed yield in soybean. Plant Biotechnol J 20:103–115

    Article  PubMed  CAS  Google Scholar 

  • Yuan S, Li Z, Li D, Yuan N, Hu Q, Luo H (2015) Constitutive expression of rice microRNA528 alters plant development and enhances tolerance to salinity stress and nitrogen starvation in creeping bentgrass. Plant Physiol 169:576–593

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan S, Zhao J, Li Z, Hu Q, Yuan N, Zhou M, Xia X, Noorai R, Saski C, Li S, Luo H (2019) MicroRNA396-mediated alteration in plant development and salinity stress response in creeping bentgrass. Hortic Res 6:48

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Wang X (2017) One new kind of phytohormonal signaling integrator: up-and-coming GASA family genes. Plant Signal Behav 12:e1226453

    Article  PubMed  Google Scholar 

  • Zhou M, Li D, Li Z, Hu Q, Yang C, Zhu L, Luo H (2013a) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol 161:1375–1391

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou Z, Sun L, Zhao Y, An L, Yan A, Meng X, Gan Y (2013b) Zinc Finger Protein 6 (ZFP6) regulates trichome initiation by integrating gibberellin and cytokinin signaling in Arabidopsis thaliana. New Phytol 198:699–708

    Article  PubMed  CAS  Google Scholar 

Download references

Funding

This project was supported by the Natural Science Foundation of Hebei Province (C2021204010), the Local Science and Technology Development Fund Projects Guided by the Central Government (236Z6302G), the State Key Laboratory of North China Crop Improvement and Regulation (NCCIR2021ZZ-17), the Research Project of Basic Scientific Research Business Fees in Provincial Universities of Hebei Province (KY2022102), Outstanding Youth Fund of Hebei Natural Science Foundation (C2022204010), and Biotechnology Risk Assessment Grant Program competitive Grant Nos. 2019-33522-30102 and 2021-33522-35342 from the USDA National Institute of Food and Agriculture.

Author information

Authors and Affiliations

  1. College of Agronomy, Hebei Agricultural University, Baoding, Hebei, 071001, People’s Republic of China

    Chang Liu, Kangting Dong, Hui Du, Jianmiao Sun & Xinbo Sun

  2. State Key Laboratory of North China Crop Improvement and Regulation, Hebei Agricultural University, Baoding, Hebei, 071001, People’s Republic of China

    Chang Liu, Kangting Dong, Hui Du, Xiaodong Wang, Jianmiao Sun & Xinbo Sun

  3. Key Laboratory of Crop Growth Regulation of Hebei Province, Hebei Agricultural University, Baoding, Hebei, 071001, People’s Republic of China

    Chang Liu, Kangting Dong, Hui Du, Jianmiao Sun & Xinbo Sun

  4. College of Plant Protection, Hebei Agricultural University, Baoding, 071000, China

    Xiaodong Wang

  5. Department of Genetics and Biochemistry, Clemson University, 110 Biosystems Research Complex, Clemson, SC, 29634, USA

    Qian Hu & Hong Luo

Authors
  1. Chang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kangting Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hui Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaodong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianmiao Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qian Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xinbo Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XS and HL conceived and designed the experiments. CL, KD, HD, JS conducted experiments. XS, XW, HD and QH analyzed the data. XS and HL wrote the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Hong Luo or Xinbo Sun.

Ethics declarations

Conflict of interests

The authors declare that they have no conflict of interests.

Additional information

Communicated by Prakash P. Kumar.

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.

Supplementary file1 (DOCX 58 KB)

Supplementary file2 (PPTX 4864 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, C., Dong, K., Du, H. et al. AsHSP26.2, a creeping bentgrass chloroplast small heat shock protein positively regulates plant development. Plant Cell Rep 43, 32 (2024). https://doi.org/10.1007/s00299-023-03109-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00299-023-03109-3

Keywords

Search

Navigation