Skip to main content
Log in

Heat-induced RING/U-BOX E3 ligase, TaUHS, is a negative regulator by facilitating TaLSD degradation during the grain filling period in wheat

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Heat stress accelerates abnormal maturation and leads to numerous defects in wheat. Temperature determines the duration of plant growth and heat stress accelerates crop development, resulting in premature initiation of phenological stages. The grain filling period is sensitive and is easily exposed to heat stress, which reduces the grain weight and shortens the period. In this study, from anthesis through early spike maturity, we observed decreased grain weight and accelerated maturation under heat stress, resulting in poor grain development. Furthermore, the maturation of spikes was accelerated to shorten the grain filling and ripening periods under high temperatures. Triticum aestivum L. UBOX responding Heat Stress gene (TaUHS) (TraesCS1D02G145900, UBOX response heat stress) was highly expressed in grains located at the basal positions of the spike under high-temperature stress. TaUHS is an E3 ligase found in the nucleus and plasma membrane. We demonstrated that TaUHS interacts with Triticum aestivum L. LEA containing seed development gene (TaLSD) (TraesCS5A02G385600, LEA-containing seed development). TaLSD, which played stress resistance and desiccation tolerance at grain filling period, mediates ubiquitination and proteasomal degradation by 26S proteasome with TaUHS under high-temperature conditions. Proteolysis of TaLSD in conjugate with E3 ligase might occur to maintain cellular homeostasis and stability in response to unfavorable environmental conditions. Wheat RING/U-BOX E3 ligase negatively regulates late embryogenesis-abundant proteins during the grain filling period under heat stress.

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

Access this article

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

Instant access to the full article PDF.

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 FASTQ fles of raw data were uploaded to the NCBI Sequence Read Archive (SRA), and the SRA study accession is PRJNA877088.

References

  • Anders S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169

    Article  CAS  PubMed  Google Scholar 

  • Angelovici R, Galili G, Fernie AR, Fait A (2010) Seed desiccation: a bridge between maturation and germination. Trends Plant Sci 15(4):211–218

    Article  CAS  PubMed  Google Scholar 

  • Bu Q, Li H, Zhao Q, Jiang H, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Wang D (2009) The Arabidopsis RING finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development. Plant Physiol 150(1):463–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Candat A, Paszkiewicz G, Neveu M, Gautier R, Logan DC, Avelange-Macherel M-H, Macherel D (2014) The ubiquitous distribution of late embryogenesis abundant proteins across cell compartments in Arabidopsis offers tailored protection against abiotic stress. Plant Cell 26(7):3148–3166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan S-P, Kao D-I, Tsai W-Y, Cheng S-C (2003) The Prp19p-associated complex in spliceosome activation. Science 302(5643):279–282

    Article  CAS  PubMed  Google Scholar 

  • Chauhan H, Khurana N, Tyagi AK, Khurana JP, Khurana P (2011) Identification and characterization of high temperature stress responsive genes in bread wheat (Triticum aestivum L.) and their regulation at various stages of development. Plant Mol Biol 75(1):35–51

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Nelson R, Sherwood J (1994) Enhanced recovery of transformants of Agrobacterium tumefaciens after freeze-thaw transformation and drug selection. Biotechniques 16(4):664–668

    CAS  PubMed  Google Scholar 

  • Chen L, Wang Z, Li M, Ma X, Tian E, Sun A, Yin Y (2018) Analysis of the natural dehydration mechanism during middle and late stages of wheat seeds development by some physiological traits and iTRAQ-based proteomic. J Cereal Sci 80:102–110

    Article  CAS  Google Scholar 

  • Ciechanover A (1998) The ubiquitin–proteasome pathway: on protein death and cell life. EMBO J 17(24):7151–7160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11(1):1–6

    Article  Google Scholar 

  • Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54(1):579–599

    Article  CAS  PubMed  Google Scholar 

  • Dias A, Lidon F (2009) Evaluation of grain filling rate and duration in bread and durum wheat, under heat stress after anthesis. J Agron Crop Sci 195(2):137–147

    Article  Google Scholar 

  • Dreccer MF, Wockner KB, Palta JA, McIntyre CL, Borgognone MG, Bourgault M, Reynolds M, Miralles DJ (2014) More fertile florets and grains per spike can be achieved at higher temperature in wheat lines with high spike biomass and sugar content at booting. Funct Plant Biol 41(5):482–495

    Article  CAS  PubMed  Google Scholar 

  • Du L, Li N, Chen L, Xu Y, Li Y, Zhang Y, Li C, Li Y (2014) The ubiquitin receptor DA1 regulates seed and organ size by modulating the stability of the ubiquitin-specific protease UBP15/SOD2 in Arabidopsis. Plant Cell 26(2):665–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan J, Cai W (2012) OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. PLoS ONE 7(9):e45117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dure L III, Greenway SC, Galau GA (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry 20(14):4162–4168

    Article  CAS  PubMed  Google Scholar 

  • Dure L, Crouch M, Harada J, Ho T-HD, Mundy J, Quatrano R, Thomas T, Sung Z (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12(5):475–486

    Article  CAS  PubMed  Google Scholar 

  • Farooq M, Bramley H, Palta JA, Siddique KH (2011) Heat stress in wheat during reproductive and grain-filling phases. Crit Rev Plant Sci 30(6):491–507

    Article  Google Scholar 

  • Fischer R, Byerlee D (1991) Trends of wheat production in warmer areas: issues and economic consideration. Wheat for non-traditional, warm areas. CIMMYT, Mexico, p 322

    Google Scholar 

  • Gallardo P, Real-Calderón P, Flor-Parra I, Salas-Pino S, Daga RR (2020) Acute heat stress leads to reversible aggregation of nuclear proteins into nucleolar rings in fission yeast. Cell Rep 33(6):108377

    Article  CAS  PubMed  Google Scholar 

  • Goel A, Goel AK, Sheoran IS (2003) Changes in oxidative stress enzymes during artificial ageing in cotton (Gossypium hirsutum L.) seeds. J Plant Physiol 160(9):1093–1100

    Article  CAS  PubMed  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388(1):151–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halford NG, Curtis TY, Chen Z, Huang J (2015) Effects of abiotic stress and crop management on cereal grain composition: implications for food quality and safety. J Exp Bot 66(5):1145–1156

    Article  CAS  PubMed  Google Scholar 

  • Hatakeyama S, Yada M, Matsumoto M, Ishida N, Nakayama K-I (2001) U box proteins as a new family of ubiquitin-protein ligases. J Biol Chem 276(35):33111–33120

    Article  CAS  PubMed  Google Scholar 

  • Henriques J, Moustacchi E (1980) Isolation and characterization of pso mutants sensitive to photo-addition of psoralen derivatives in Saccharomyces cerevisiae. Genetics 95(2):273–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong MJ, Kim J-B, Seo YW, Kim DY (2021) Regulation of glycosylphosphatidylinositol-anchored protein (GPI-AP) expression by F-Box/LRR-repeat (FBXL) protein in wheat (Triticum aestivum L.). Plants 10(8):1606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houde M, Dallaire S, N’Dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol J 2(5):381–387

    Article  CAS  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Biol 47(1):377–403

    Article  CAS  Google Scholar 

  • Kaur M, Bhagi P, Gupta AK, Zhawar VK (2013) Antioxidant potential and expression of Lea genes under heat stress in two wheat cultivars differing in heat tolerance. Plant Stress 7(1):19–29

    Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim DY, Lee YJ, Hong MJ, Kim JH, Seo YW (2021a) Genome wide analysis of U-box E3 ubiquitin ligases in wheat (Triticum aestivum L.). Int J Mol Sci 22(5):2699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JH, Khan IU, Lee CW, Kim DY, Jang CS, Lim SD, Park YC, Kim JH, Seo YW (2021b) Identification and analysis of a differentially expressed wheat RING-type E3 ligase in spike primordia development during post-vernalization. Plant Cell Rep 40(3):543–558

    Article  CAS  PubMed  Google Scholar 

  • Kim JH, Lee JE, Jang CS (2021c) Regulation of Oryza sativa molybdate transporter1; 3 degradation via RING finger E3 ligase OsAIR3. J Plant Physiol 264:153484

    Article  CAS  PubMed  Google Scholar 

  • Ko CS, Kim J-B, Hong MJ, Seo YW (2021) Wheat (Triticum aestivum L.) TaHMW1D transcript variants are highly expressed in response to heat stress and in grains located in distal part of the spike. Plants 10(4):687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147(1):381–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurepa J, Toh-e A, Smalle JA (2008) 26S proteasome regulatory particle mutants have increased oxidative stress tolerance. Plant J 53(1):102–114

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22(10):1331–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ling H, Zeng X, Guo S (2016) Functional insights into the late embryogenesis abundant (LEA) protein family from Dendrobium officinale (Orchidaceae) using an Escherichia coli system. Sci Rep 6(1):1–9

    Article  Google Scholar 

  • Love M, Anders S, Huber W (2016) DESeq2 vignette. Genome Biol 15:110

    Google Scholar 

  • Makarov EM, Makarova OV, Urlaub H, Gentzel M, Will CL, Wilm M, Lührmann R (2002) Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 298(5601):2205–2208

    Article  CAS  PubMed  Google Scholar 

  • Manfre AJ, Lanni LM, Marcotte WR Jr (2006) The Arabidopsis group 1 LATE EMBRYOGENESIS ABUNDANT protein ATEM6 is required for normal seed development. Plant Physiol 140(1):140–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng L, Feldman L (2010) A rapid TRIzol-based two-step method for DNA-free RNA extraction from Arabidopsis siliques and dry seeds. Wiley

    Book  Google Scholar 

  • NDong C, Danyluk J, Wilson KE, Pocock T, Huner NP, Sarhan F (2002) Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Molecular characterization and functional analyses. Plant Physiol 129(3):1368–1381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson SK, Ariizumi T, Steber CM (2017) Biology in the dry seed: transcriptome changes associated with dry seed dormancy and dormancy loss in the Arabidopsis GA-insensitive sleepy1-2 mutant. Front Plant Sci 8:2158

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicolas ME, Gleadow RM, Dalling MJ (1984) Effects of drought and high temperature on grain growth in wheat. Funct Plant Biol 11(6):553–566

    Article  Google Scholar 

  • Ohi R, McCollum D, Hirani B, Den Haese G, Zhang X, Burke J, Turner K, Gould K (1994) The Schizosaccharomyces pombe cdc5+ gene encodes an essential protein with homology to c-Myb. EMBO J 13(2):471–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohi MD, Vander Kooi CW, Rosenberg JA, Chazin WJ, Gould KL (2003) Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat Struct Mol Biol 10(4):250–255

    Article  CAS  Google Scholar 

  • Olvera-Carrillo Y, Campos F, Reyes JL, Garciarrubio A, Covarrubias AA (2010) Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabidopsis. Plant Physiol 154(1):373–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palma K, Zhao Q, Cheng YT, Bi D, Monaghan J, Cheng W, Zhang Y, Li X (2007) Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms. Genes Dev 21(12):1484–1493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasad PV, Pisipati S, Ristic Z, Bukovnik U, Fritz A (2008) Impact of nighttime temperature on physiology and growth of spring wheat. Crop Sci 48(6):2372–2380

    Article  Google Scholar 

  • Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69(3):225–232

    Article  Google Scholar 

  • Saini H, Aspinall D (1982) Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature. Ann Bot 49(6):835–846

    Article  Google Scholar 

  • Serrano I, Campos L, Rivas S (2018) Roles of E3 ubiquitin-ligases in nuclear protein homeostasis during plant stress responses. Front Plant Sci 9:139

    Article  PubMed  PubMed Central  Google Scholar 

  • Sofield I, Evans L, Cook M, Wardlaw IF (1977) Factors influencing the rate and duration of grain filling in wheat. Funct Plant Biol 4(5):785–797

    Article  Google Scholar 

  • Song X-J, Huang W, Shi M, Zhu M-Z, Lin H-X (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39(5):623–630

    Article  CAS  PubMed  Google Scholar 

  • Song EJ, Werner SL, Neubauer J, Stegmeier F, Aspden J, Rio D, Harper JW, Elledge SJ, Kirschner MW, Rape M (2010) The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev 24(13):1434–1447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki N (2016) Hormone signaling pathways under stress combinations. Plant Signal Behav 11(11):e1247139

    Article  PubMed  PubMed Central  Google Scholar 

  • Tashiro T, Wardlaw IF (1989) A comparison of the effect of high temperature on grain development in wheat and rice. Ann Bot 64(1):59–65

    Article  Google Scholar 

  • Teixeira EI, Fischer G, Van Velthuizen H, Walter C, Ewert F (2013) Global hot-spots of heat stress on agricultural crops due to climate change. Agric for Meteorol 170:206–215

    Article  Google Scholar 

  • Tewolde H, Fernandez C, Erickson C (2006) Wheat cultivars adapted to post-heading high temperature stress. J Agron Crop Sci 192(2):111–120

    Article  Google Scholar 

  • Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94(10):791–812

    Article  CAS  PubMed  Google Scholar 

  • Vander Kooi CW, Ren L, Xu P, Ohi MD, Gould KL, Chazin WJ (2010) The Prp19 WD40 domain contains a conserved protein interaction region essential for its function. Structure 18(5):584–593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vierstra RD (2009) The ubiquitin–26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10(6):385–397

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Wang R, Mao X, Zhang J, Liu Y, Xie Q, Yang X, Chang X, Li C, Zhang X (2020) RING finger ubiquitin E3 ligase gene TaSDIR1-4A contributes to determination of grain size in common wheat. J Exp Bot 71(18):5377–5388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West M, Harada JJ (1993) Embryogenesis in higher plants: an overview. Plant Cell 5(10):1361

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia T, Li N, Dumenil J, Li J, Kamenski A, Bevan MW, Gao F, Li Y (2013) The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell 25(9):3347–3359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Zhang Y, Guan Z, Wei W, Han L, Chai T (2008) Expression and function of two dehydrins under environmental stresses in Brassica juncea L. Mol Breeding 21(4):431–438

    Article  CAS  Google Scholar 

  • Xu L, Ménard R, Berr A, Fuchs J, Cognat V, Meyer D, Shen WH (2009) The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J 57(2):279–288

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi H, Hsu J, Hung M-C (2012) Regulation of ubiquitination-mediated protein degradation by survival kinases in cancer. Front Oncol 2:15

    Article  PubMed  PubMed Central  Google Scholar 

  • Yassin M, Fara SA, Hossain A, Saneoka H, El Sabagh A (2019) Assessment of salinity tolerance bread wheat genotypes: using stress tolerance indices. Fresenius Environ Bull 28(5):4199–4217

    CAS  Google Scholar 

  • Yee D, Goring DR (2009) The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J Exp Bot 60(4):1109–1121

    Article  CAS  PubMed  Google Scholar 

  • Zahedi M, Jenner CF (2003) Analysis of effects in wheat of high temperature on grain filling attributes estimated from mathematical models of grain filling. J Agric Sci 141(2):203–212

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a Korea University grant.

Funding

Funding was provided by Cooperative Research Program for Agriculture Science & Technology Development (Grant No. PJ015705), Basic Science Research Program through the National Research Foundation of Korea (Grant No. 2019R1I1A1A01059968, NRF), Ministry of Science, ICT & Future Planning (Grant No. 2017R1D1A1B06030349).

Author information

Authors and Affiliations

Authors

Contributions

CSK and YWS conceived and designed the study. CSK and J-BK designed the experiments to treat the plants. CSK, JSL, and MJH conducted the experiments. CSK and DYK contributed to analytical tools. CSK analyzed the data and wrote the first draft of the manuscript. All authors commented on previous versions of the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Yong Weon Seo.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Communicated by Guoping Zhang.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor 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

Ko, C.S., Kim, D.Y., Lee, J.S. et al. Heat-induced RING/U-BOX E3 ligase, TaUHS, is a negative regulator by facilitating TaLSD degradation during the grain filling period in wheat. Plant Growth Regul 99, 251–264 (2023). https://doi.org/10.1007/s10725-022-00902-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-022-00902-0

Keywords

Navigation