Skip to main content
SpringerLink
Log in

Differential responses of anthers of stress tolerant and sensitive wheat cultivars to high temperature stress

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Transcriptomic analyses identified anther-expressed genes in wheat likely to contribute to heat tolerance and hence provide useful genetic markers. The genes included those involved in hormone biosynthesis, signal transduction, the heat shock response and anther development.

Abstract

Pollen development is particularly sensitive to high temperature heat stress. In wheat, heat-tolerant and heat-sensitive cultivars have been identified, although the underlying genetic causes for these differences are largely unknown. The effects of heat stress on the developing anthers of two heat-tolerant and two heat-sensitive wheat cultivars were examined in this study. Heat stress (35 °C) was found to disrupt pollen development in the two heat-sensitive wheat cultivars but had no visible effect on pollen or anther development in the two heat-tolerant cultivars. The sensitive anthers exhibited a range of developmental abnormalities including an increase in unfilled and clumped pollen grains, abnormal pollen walls and a decrease in pollen viability. This subsequently led to a greater reduction in grain yield in the sensitive cultivars following heat stress. Transcriptomic analyses of heat-stressed developing wheat anthers of the four cultivars identified a number of key genes which may contribute to heat stress tolerance during pollen development. Orthologs of some of these genes in Arabidopsis and rice are involved in regulation of the heat stress response and the synthesis of auxin, ethylene and gibberellin. These genes constitute candidate molecular markers for the breeding of heat-tolerant wheat lines.

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
Fig. 9

Similar content being viewed by others

Data availability

The transcriptomic sequences utilised in this study have been deposited at the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) under the Bioproject IDs PRJNA433429 and PRJNA638225.

Abbreviations

GO:

Gene ontology

FDA:

Fluorescein diacetate

FDR:

False discovery rate

HSF:

Heat shock factor

HSP:

Heat shock protein

PCD:

Programmed cell death

PI:

Propidium iodide

SEM:

Scanning electron microscope

References

  • Abiko M, Akibayashi K, Sakata T, Kimura M, Kihara M, Itoh K, Asamizu E, Sato S, Takahashi H, Higashitani A (2005) High-temperature induction of male sterility during barley (Hordeum vulgare L.) anther development is mediated by transcriptional inhibition. Sex Plant Reprod 18(2):91–100

    CAS  Google Scholar 

  • Alexa A, Rahnenfuhrer J (2010) topGO: enrichment analysis for gene ontology. R package version 2

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Andrews S (2010) FastQC: a quality control tool for high throughput sequence data

  • Anwar MR, O’leary G, McNeil D, Hossain H, Nelson R (2007) Climate change impact on rainfed wheat in south-eastern Australia. Field Crops Res 104:139–147

    Google Scholar 

  • Appels R, Eversole K, Feuillet C et al (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361(6403):eaar7191

    Google Scholar 

  • Asseng S, Ewert F, Martre P et al (2015) Rising temperatures reduce global wheat production. Nat Clim Chang 5:143–147

    Google Scholar 

  • Aviezer-Hagai K, Skovorodnikova J, Galigniana M, Farchi-Pisanty O, Maayan E, Bocovza S et al (2007) Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol Biol 63(2):237–255

    CAS  PubMed  Google Scholar 

  • Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21(5):1453–1472

    CAS  PubMed  PubMed Central  Google Scholar 

  • Balfagón D, Sengupta S, Gómez-Cadenas A, Fritschi FB, Azad RK, Mittler R et al (2019) Jasmonic acid is required for plant acclimation to a combination of high light and heat stress. Plant Physiol 181(4):1668–1682

    PubMed  PubMed Central  Google Scholar 

  • Barnabás B, Jäger K, Fehér A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38

    PubMed  Google Scholar 

  • Begcy K, Nosenko T, Zhou L-Z, Fragner L, Weckwerth W, Dresselhaus T (2019) Male sterility in maize after transient heat stress during the tetrad stage of pollen development. Plant Physiol 181:683–700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bita C, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273

    PubMed  PubMed Central  Google Scholar 

  • Bokszczanin KL, Fragkostefanakis S (2013) Perspectives on deciphering mechanisms underlying ant heat stress response and thermotolerance Solanaceae Pollen Thermotolerance Initial Training Network (SPOT-ITN) Consortium. Front Plant Sci 4:315

    PubMed  PubMed Central  Google Scholar 

  • Bourbousse C, Vegesna N, Law JA (2018) SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis. Proc Natl Acad Sci USA 115(52):E12453–E12462

    CAS  PubMed  PubMed Central  Google Scholar 

  • Browne RG, Iacuone S, Li SF, Dolferus R, Parish RW (2018) Anther morphological development and stage determination in Triticum aestivum. Front Plant Sci 9:228

    PubMed  PubMed Central  Google Scholar 

  • Bryant DM, Johnson K, DiTommaso T et al (2017) A tissue-mapped axolotl de novo transcriptome enables identification of limb regeneration factors. Cell Rep 18:762–776

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cai C-F, Zhu J, Lou Y, Guo Z-L, Xiong S-X, Wang K, Yang Z-N (2015) The functional analysis of OsTDF1 reveals a conserved genetic pathway for tapetal development between rice and Arabidopsis. Sci Bull 60:1073–1082

    CAS  Google Scholar 

  • Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143(1):251–262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Hwang JE, Lim CJ, Kim DY, Lee SY, Lim CO et al (2010) Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem Biophys Res Commun 401(2):238–244

    CAS  PubMed  Google Scholar 

  • Comastri A, Janni M, Simmonds J, Uauy C, Pignone D, Nguyen HT, Marmiroli N (2018) Heat in wheat: exploit reverse genetic techniques to discover new alleles within the Triticum durum sHsp26 family. Front Plant Sci 9:1337

    PubMed  PubMed Central  Google Scholar 

  • Consortium GO (2016) Expansion of the gene ontology knowledgebase and resources. Nucleic Acids Res 45:D331–D338

    Google Scholar 

  • Consortium U (2016) UniProt: the universal protein knowledgebase. Nucleic Acids Res 45:D158–D169

    Google Scholar 

  • Dahlke RI, Fraas S, Ullrich KK et al (2017) Protoplast swelling and hypocotyl growth depend on different auxin signaling pathways. Plant Physiol 175(2):982–994

    PubMed  PubMed Central  Google Scholar 

  • Dai N, Wang W, Patterson SE, Bleecker AB (2013) The TMK subfamily of receptor-like kinases in Arabidopsis display an essential role in growth and a reduced sensitivity to auxin. PLoS ONE 8:60990

    Google Scholar 

  • Dolferus R, Ji X, Richards RA (2011) Abiotic stress and control of grain number in cereals. Plant Sci 181:331–341

    CAS  PubMed  Google Scholar 

  • Doukhanina EV, Chen S, van der Zalm E, Godzik A, Reed J, Dickman MB (2006) Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J Biol Chem 281(27):18793–18801

    CAS  PubMed  Google Scholar 

  • Feng M, Kim J-Y (2015) Revisiting apoplastic auxin signaling mediated by AUXIN BINDING PROTEIN 1. Mol Cells 38(10):829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feng B, Zhang C, Chen T, Zhang X, Tao L, Fu G (2018) Salicylic acid reverses pollen abortion of rice caused by heat stress. BMC Plant Biol 18:245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Bateman A, Clements J et al (2013) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230

    PubMed  PubMed Central  Google Scholar 

  • Firon N, Pressman E, Meir S, Khoury R, Altahan L (2012) Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB Plants 2012:pls024

    PubMed  PubMed Central  Google Scholar 

  • Fragkostefanakis S, Roth S, Schleiff E, Scharf K-D (2015) Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant Cell Environ 38:1881–1895

    CAS  PubMed  Google Scholar 

  • Fu Z, Yu J, Cheng X, Zong X, Xu J, Chen M, Li Z, Zhang D, Liang W (2014) The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell 26:1512–1524

    CAS  PubMed  PubMed Central  Google Scholar 

  • Godfray HCJ, Beddington JR, Crute IR et al (2010) Food security: the challenge of feeding 9 billion people. Science 327(5967):812–818

    CAS  PubMed  Google Scholar 

  • Gómez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57(11):876–891

    PubMed  PubMed Central  Google Scholar 

  • González-Schain N, Dreni L, Lawas LM, Galbiati M, Colombo L, Heuer S, Jagadish KS, Kater MM (2015) Genome-wide transcriptome analysis during anthesis reveals new insights into the molecular basis of heat stress responses in tolerant and sensitive rice varieties. Plant Cell Physiol 57:57–68

    PubMed  Google Scholar 

  • Gothandam KM, Kim ES, Chung YY (2007) Ultrastructural study of rice tapetum under low-temperature stress. J Plant Biol 50:396–402

    Google Scholar 

  • Gowda NKC, Kandasamy G, Froehlich MS, Dohmen RJ, Andréasson C (2013) Hsp70 nucleotide exchange factor Fes1 is essential for ubiquitin-dependent degradation of misfolded cytosolic proteins. Proc Natl Acad Sci USA 110(15):5975–5980

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haas B, Papanicolaou A (2016) TransDecoder (find coding regions within transcripts). GitHub Inc

    Google Scholar 

  • Higashitani A (2013) High temperature injury and auxin biosynthesis in microsporogenesis. Front Plant Sci 4:47

    PubMed  PubMed Central  Google Scholar 

  • Hong S-W, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97(8):4392–4397

    CAS  PubMed  PubMed Central  Google Scholar 

  • Innes P, Tan D, Van Ogtrop F, Amthor J (2015) Effects of high-temperature episodes on wheat yields in New South Wales, Australia. Agric for Meteorol 208:95–107

    Google Scholar 

  • Jagadish SV, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot 61(1):143–156

    CAS  PubMed  Google Scholar 

  • Je J, Song C, Hwang JE, Chung WS, Lim CO (2014) DREB2C acts as a transcriptional activator of the thermo tolerance-related phytocystatin 4 (AtCYS4) gene. Transgenic Res 23:109–123

    CAS  PubMed  Google Scholar 

  • Jiang Y, Lahlali R, Karunakaran C, Kumar S, Davis AR, Bueckert RA (2015) Seed set, pollen morphology and pollen surface composition response to heat stress in field pea. Plant Cell Environ 38(11):2387–2397

    CAS  PubMed  Google Scholar 

  • Jones KH, Senft JA (1985) An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J Histochem Cytochem 33:77–79

    CAS  PubMed  Google Scholar 

  • Kersey PJ, Allen JE, Armean I et al (2016) Ensembl Genomes 2016: more genomes, more complexity. Nucleic Acids Res 44:D574–D580

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kloth KJ, Wiegers GL, Busscher-Lange J, van Haarst JC, Kruijer W, Bouwmeester HJ, Dicke M, Jongsma MA (2016) AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling. J Exp Bot 67:3383–3396

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kotak S, Vierling E, Bäumlein H, von Koskull-Döring P (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19(1):182–195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krogh A, Larsson B, Von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    CAS  PubMed  Google Scholar 

  • Krueger F (2015) Trim Galore!: A wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files. GitHub Inc, USA

    Google Scholar 

  • Kumar N, Kumar N, Shukla A, Shankhdhar SC, Shankhdhar D (2015) Impact of terminal heat stress on pollen viability and yield attributes of rice (Oryza sativa L.). Cereal Res Commun 43(4):616–626

    CAS  Google Scholar 

  • Lämke J, Brzezinka K, Bäurle I (2016) HSFA2 orchestrates transcriptional dynamics after heat stress in Arabidopsis thaliana. Transcription 7(4):111–114

    PubMed  PubMed Central  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    PubMed  PubMed Central  Google Scholar 

  • Li D-D, Xue J-S, Zhu J, Yang Z-N (2017) Gene regulatory network for tapetum development in Arabidopsis thaliana. Front Plant Sci 8:1559

    PubMed  PubMed Central  Google Scholar 

  • Lohani N, Singh MB, Bhalla PL (2020) High temperature susceptibility of sexual reproduction in crop plants. J Exp Bot 71:555–568

    CAS  PubMed  Google Scholar 

  • Lou Y, Zhou HS, Han Y, Zeng QY, Zhu J, Yang ZN (2018) Positive regulation of AMS by TDF1 and the formation of a TDF1–AMS complex are required for anther development in Arabidopsis thaliana. New Phytol 217:378–391

    CAS  PubMed  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

    PubMed  PubMed Central  Google Scholar 

  • Lu P-P, Zheng W-J, Wang C-T et al (2018) Wheat Bax Inhibitor-1 interacts with TaFKBP62 and mediates response to heat stress. BMC Plant Biol 18:259

    CAS  PubMed  PubMed Central  Google Scholar 

  • Masoomi-Aladizgeh F, Najeeb U, Hamzelou S, Pascovici D, Amirkhani A, Tan DKY, Mirzaui M, Haynes PA, Atwell BJ (2020) Pollen development in cotton (Gossypium hirsutum) is highly sensitive to heat exposure during the tetrad stage. Plant Cell Environ. https://doi.org/10.1111/pce.13908

    Article  PubMed  Google Scholar 

  • Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90. 1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59(3):387–399

    CAS  PubMed  Google Scholar 

  • Mesihovic A, Iannacone R, Firon N, Fragkostefanakis S (2016) Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reprod 29:93–105

    CAS  PubMed  Google Scholar 

  • Nan G-L, Zhai J, Arikit S, Morrow D, Fernandes J, Mai L et al (2017) MS23, a master basic helix-loop-helix factor, regulates the specification and development of the tapetum in maize. Development 144(1):163–172

    CAS  PubMed  Google Scholar 

  • Ni Z, Li H, Zhao Y, Peng H, Hu Z, Xin M, Sun Q (2018) Genetic improvement of heat tolerance in wheat: recent progress in understanding the underlying molecular mechanisms. Crop J 6(1):32–34

    Google Scholar 

  • Niu N, Liang W, Yang X, Jin W, Wilson ZA, Hu J, Zhang D (2013) EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat Commun 4:1445

    PubMed  Google Scholar 

  • Ohama N, Kusakabe K, Mizoi J, Zhao H, Kidokoro S, Koizumi S, Takahashi F, Ishida T, Yanagisawa S, Shinozaki K, Yamaguchi-Shinozaki K (2016) The transcriptional cascade in the heat stress response of Arabidopsis is strictly regulated at the level of transcription factor expression. Plant Cell 28(1):181–201

    CAS  PubMed  Google Scholar 

  • Oliveros JC (2015) Venny. An interactive tool for comparing lists with Venn's diagrams. https://bioinfogp.cnb.csic.es/tools/venny/index.html

  • Oshino T, Abiko M, Saito R, Ichiishi E, Endo M, Kawagishi-Kobayashi M, Higashitani A (2007) Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol Genet Genom 278:31–42

    CAS  Google Scholar 

  • Oshino T, Miura S, Kikuchi S, Hamada K, Yano K, Watanabe M et al (2011) Auxin depletion in barley plants under high-temperature conditions represses DNA proliferation in organelles and nuclei via transcriptional alterations. Plant Cell Environ 34(2):284–290

    CAS  PubMed  Google Scholar 

  • Pan X, Yan W, Chang Z, Xu Y, Luo M, Xu C, Chen Z, Wu J, Tang X (2020) OsMYB80 regulates anther development and pollen fertility by targeting multiple biological pathways. Plant Cell Physiol 61:988–1004

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parish RW, Phan HA, Iacuone S, Li SF (2012) Tapetal development and abiotic stress: a centre of vulnerability. Funct Plant Biol 39:553–559

    CAS  PubMed  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785

    CAS  PubMed  Google Scholar 

  • Phan HA, Li SF, Parish RW (2012) MYB80, a regulator of tapetal and pollen development, is functionally conserved in crops. Plant Mol Biol 78:171–183

    CAS  PubMed  Google Scholar 

  • Plackett AR, Ferguson AC, Powers SJ, Wanchoo-Kohli A, Phillips AL, Wilson ZA, Hedden P, Thomas SG (2014) DELLA activity is required for successful pollen development in the Columbia ecotype of Arabidopsis. New Phytol 201(3):825–836

    CAS  PubMed  Google Scholar 

  • Qin D, Wang F, Geng X, Zhang L, Yao Y, Ni Z et al (2015) Overexpression of heat stress-responsive TaMBF1c, a wheat (Triticum aestivum L.) multiprotein bridging factor, confers heat tolerance in both yeast and rice. Plant Mol Biol 87(1–2):31–45

    CAS  PubMed  Google Scholar 

  • Rieu I, Twell D, Firon N (2017) Pollen development at high temperature: from acclimation to collapse. Plant Physiol 173(4):1967–1976

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Saini H, Sedgley M, Aspinall D (1984) Development anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid. Funct Plant Biol 11:243–253

    Google Scholar 

  • Sakata T, Oshino T, Miura S et al (2010) Auxins reverse plant male sterility caused by high temperatures. Proc Natl Acad Sci USA 107:8569–8574

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schauberger B, Archontoulis S, Arneth A et al (2017) Consistent negative response of US crops to high temperatures in observations and crop models. Nat Commun 8:13931

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R (2011) Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J 66(5):844–851

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wardlaw I, Dawson I, Munibi P, Fewster R (1989) The tolerance of wheat to high temperatures during reproductive growth. I. Survey procedures and general response patterns. Aust J Agric Res 40:1–13

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Xu T, Dai N, Chen J et al (2014a) Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343(6174):1025–1028

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Iacuone S, Li SF, Parish RW (2014b) MYB80 homologues in Arabidopsis, cotton and Brassica: regulation and functional conservation in tapetal and pollen development. BMC Plant Biol 14:278

    PubMed  PubMed Central  Google Scholar 

  • Xue G-P, Drenth J, McIntyre CL (2015) TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets. J Exp Bot 66:1025–1039

    CAS  PubMed  Google Scholar 

  • Yamagami A, Saito C, Nakazawa M et al (2017) Evolutionarily conserved BIL4 suppresses the degradation of brassinosteroid receptor BRI1 and regulates cell elongation. Sci Rep 7:5739

    PubMed  PubMed Central  Google Scholar 

  • Yao X, Tian L, Yang J, Zhao Y-N, Zhu Y-X, Dai X et al (2018) Auxin production in diploid microsporocytes is necessary and sufficient for early stages of pollen development. PLoS Genet 14(5):e1007397

    PubMed  PubMed Central  Google Scholar 

  • Ye Q, Zhu W, Li L, Zhang S, Yin Y, Ma H et al (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc Natl Acad Sci USA 107(13):6100–6105

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S-S, Yang H, Ding L, Song Z-T, Ma H, Liu JX (2017) Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in Arabidopsis. Plant Cell 29:1007–1025

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the assistance of Dr. Peter Lock and the LIMS BioImaging Facility for training and Scanning electron microscope usage and the La Trobe University Genomics Platform for training and assistance with transcriptomic analyses. We also thank Sue Kleven and Xiaomei Wallace for excellent technical assistance for growing wheat plants and for sterility counting. This work was supported by funding from the Grains Research and Development Corporation (GRDC) [project codes ULA 00009, CSP 00175].

Author information

Authors and Affiliations

  1. AgriBio, Centre for Agribioscience, Department of Animal, Plant and Soil Sciences, La Trobe University, Bundoora, VIC, Australia

    Richard G. Browne, Song F. Li, Sylvana Iacuone & Roger W. Parish

  2. Melbourne Polytechnic, Epping, VIC, Australia

    Sylvana Iacuone

  3. CSIRO Agriculture and Food, Canberra, ACT, Australia

    Rudy Dolferus

Authors
  1. Richard G. Browne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Song F. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sylvana Iacuone
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rudy Dolferus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roger W. Parish
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roger W. Parish.

Ethics declarations

Conflict of interest

No conflicts of interest were declared.

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.

425_2021_3656_MOESM1_ESM.pdf

Supplementary file1 Fig. S1 Transverse sections of anther locules at stage 10 in Halberd, Young, Cranbrook and Wyalkatchem under control conditions (22 °C/14 °C). All four cultivars have a similar developmental pattern under control conditions (Browne et al. 2018). Fig. S2 SEM images of groups of freshly prepared pollen of four wheat cultivars following three days of either control (a, c, e, g) or high temperature stress (b, d, f, h) treatment. Fig S3 Numbers of differentially expressed genes in each of the four cultivars following 12 h high temperature stress. Up-regulated, down-regulated and total number of genes for the meiosis, tetrad, and combined stage results are shown. Differentially expressed genes are those which give a False Discovery Rate < 0.01 when comparing either three (for meiosis and tetrad timepoints) or six (for combined stages) biological replicates. Comparing anthers harvested following 12 h at control (22 °C) and high temperature (35 °C) conditions. Fig. S4 Simplified model of key anther and pollen regulatory development pathway in Arabidopsis and rice. Direct regulation of one gene by another shown with black arrows. Regulation of pollen and tapetal development by pathway shown with dotted arrows. Genes included are DEFECTIVE IN TAPETAL DEVELOPMENT AND FUNCTION1 (TDF1), ABORTED MICROSPORES (AMS)/TAPETUM DEGENERATION RETARDATION (TDR), MYB80 (also known as MYB103 and MS188), MALE STERILITY1 (MS1)/PERSISTENT TAPETAL CELL1 (PTC1), TDR INTERACTING PROTEIN2 (TIP2) and ETERNAL TAPETUM1 (EAT1). Model derived using data from models in rice (Fu et al. 2014; Cai et al. 2015) and Arabidopsis (Cai et al. 2015; Li et al. 2017; Lou et al. 2018). Fig. S5 Normalised expression of TDF1 (a) and PTC1 (b) orthologs in four wheat cultivars under control (blue) and heat stress (red) conditions. (PDF 574 KB)

425_2021_3656_MOESM2_ESM.xlsx

Supplementary file2 Table S1 Pedigree information for the four wheat cultivars used in this study. Table S2 List of all genes mentioned in publication with both TGAC v1.0 and IWGSC v1.1 gene IDs for comparison. Table S3 A list of 121 genes which were up-regulated following heat stress in any of the cultivars which were assigned to the Gene Ontology term ‘response to heat’. Table S4 A list of all 72 genes that showed greater than eightfold higher expression in the two tolerant cultivars compared to the two sensitive cultivars. Table S5 A list of all 75 genes identified as being up-regulated more than eightfold following high temperature stress treatment in all four cultivars. (XLSX 25 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Browne, R.G., Li, S.F., Iacuone, S. et al. Differential responses of anthers of stress tolerant and sensitive wheat cultivars to high temperature stress. Planta 254, 4 (2021). https://doi.org/10.1007/s00425-021-03656-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-021-03656-7

Keywords

Search

Navigation