Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Synthesis of heat-shock proteins HSP-70 and HSP-90 in flowers of common buckwheat (Fagopyrum esculentum) under thermal stress

A. Płażek https://orcid.org/0000-0003-2119-5890 A , K. Hura https://orcid.org/0000-0001-5697-2886 A , T. Hura https://orcid.org/0000-0001-8537-4455 B D , A. Słomka https://orcid.org/0000-0001-5682-8323 C , M. Hornyák https://orcid.org/0000-0003-3523-7115 A and K. Sychta https://orcid.org/0000-0001-7368-1570 C
+ Author Affiliations
- Author Affiliations

A Department of Plant Breeding, Physiology and Seed Science, University of Agriculture, Podłużna 3, 30-239 Kraków, Poland.

B Polish Academy of Sciences, The Franciszek Górski Institute of Plant Physiology, Niezapominajek 21, 30-239 Kraków, Poland.

C Institute of Botany, Department of Plant Cytology and Embryology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland.

D Corresponding author. Email: t.hura@ifr-pan.edu.pl

Crop and Pasture Science 71(8) 760-767 https://doi.org/10.1071/CP20011
Submitted: 14 January 2020  Accepted: 19 June 2020   Published: 16 July 2020

Abstract

Common buckwheat (Fagopyrum esculentum Moench) is a valuable crop plant with cereal-like seed chemical composition; however, it is susceptible to thermal stress. The aim of the study was to determine whether heat-shock proteins HSP-90 and HSP-70 can protect common buckwheat against thermal stress during development of microspores and embryo sacs. The study was performed on two accessions of common buckwheat, Panda and PA15, which differed in their tolerance to thermal stress. Accumulation of these proteins was determined in buds, open and wilted flowers, and donor leaves of plants grown at 20°C (control) and 30°C (thermal stress). Photochemical efficiency of donor leaves, closest to the inflorescences, based on chlorophyll a fluorescence (ChlF) was also analysed. All plants demonstrated higher values of ChlF at 30°C than at 20°C, which suggests that this 30°C temperature is more conducive to their vegetative growth. Pollen grains of both accessions demonstrated normal development at 30°C, whereas embryo sacs showed many developmental disturbances. Panda was more sensitive to thermal stress than PA15, as manifested in a higher percentage of degenerated embryo sacs at the flower bud phase. Moreover, a decrease in both HSPs in the studied organs of Panda was found relative to the control. At 30°C, both accessions accumulated more HSP-70 than HSP-90. These results suggest that, under heat stress, HSP-70 plays a protective role for flowers of common buckwheat. The analyses indicated that the donor leaf closest to the flower cluster may be a reliable indicator of temperature sensitivity in buckwheat flowers.

Additional keywords: chlorophyll fluorescence, embryological analyses, stress tolerance, western-blot.


References

Abdelmageed AHA, Gruda N (2009) Influence of grafting on growth, development and some physiological parameters of tomatoes under controlled heat stress conditions. European Journal of Horticultural Science 74, 16–20.

Adachi T (1990) How to combine the reproductive system with biotechnology in order to overcome the breeding barrier in buckwheat. Fagopyrum 10, 7–11.

Agati G, Cerovic ZG, Moya I (2000) The effect of decreasing temperature up to chilling values on the in vivo F685/F735 chlorophyll fluorescence ratio in Phaseolus vulgaris and Pisum sativum: the role of the photosystem I contribution to the 735 nm fluorescence band. Photochemistry and Photobiology 72, 75–84.
The effect of decreasing temperature up to chilling values on the in vivo F685/F735 chlorophyll fluorescence ratio in Phaseolus vulgaris and Pisum sativum: the role of the photosystem I contribution to the 735 nm fluorescence band.Crossref | GoogleScholarGoogle Scholar | 10911731PubMed |

Allakhverdiev SI, Kreslavski VD, Klimov VV, Dmitry AL, Carpentier R (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis Research 98, 541.
Heat stress: an overview of molecular responses in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 18649006PubMed |

Baker NR (1991) A possible role for photosystem II in environmental perturbations of photosynthesis. Physiologia Plantarum 81, 563–570.
A possible role for photosystem II in environmental perturbations of photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Molecular Biology 32, 191–222.
Molecular chaperones and protein folding in plants.Crossref | GoogleScholarGoogle Scholar | 8980480PubMed |

Camejo D, Rodriguez P, Morales MA, Dell’Amico JM, Torrecillas A, Alarcón JJ (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. Journal of Plant Physiology 162, 281–289.
High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility.Crossref | GoogleScholarGoogle Scholar | 15832680PubMed |

Cao DS, Froehlich JE, Zhang H, Cheng CL (2003) The chlorate-resistant and photomorphogenesis-defensive mutant cr88 encodes a chloroplast-targeted HSP90. The Plant Journal 33, 107–118.
The chlorate-resistant and photomorphogenesis-defensive mutant cr88 encodes a chloroplast-targeted HSP90.Crossref | GoogleScholarGoogle Scholar |

Cawoy V, Deblauwe V, Halbrecq B, Ledent JM, Kinet JM, Jacquemart AL (2006) Morph differences and honeybee morph preference in the distylous species Fagopyrum esculentum Moench. International Journal of Plant Sciences 167, 853–861.
Morph differences and honeybee morph preference in the distylous species Fagopyrum esculentum Moench.Crossref | GoogleScholarGoogle Scholar |

Cawoy V, Ledent JF, Kinet JM, Jacquemart AL (2009) Floral biology of common buckwheat (Fagopyrum esculentum Moench). The European Journal of Plant Science and Biotechnology 3, 1–9.

Crosatti C, Delaureto PP, Bassi R, Cattivelli L (1999) The interaction between cold and light controls the expression of the cold-regulated barley gene cor14b and the accumulation of the corresponding protein. Plant Physiology 119, 671–680.
The interaction between cold and light controls the expression of the cold-regulated barley gene cor14b and the accumulation of the corresponding protein.Crossref | GoogleScholarGoogle Scholar | 9952464PubMed |

Edreva A (2005) Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agriculture, Ecosystems & Environment 106, 119–133.
Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach.Crossref | GoogleScholarGoogle Scholar |

Essemine J, Govindachary S, Ammar S, Bouzid S, Carpentier R (2012) Enhanced sensitivity of the photosynthetic apparatus to heat stress in digalactosyl-diacylglycerol deficient Arabidopsis. Environmental and Experimental Botany 80, 16–26.
Enhanced sensitivity of the photosynthetic apparatus to heat stress in digalactosyl-diacylglycerol deficient Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Fischer EM, Knutti R (2015) Anthropogenic contribution to global occurrence of heavy-precipitation and high-temperature extremes. Nature Climate Change 5, 560–564.
Anthropogenic contribution to global occurrence of heavy-precipitation and high-temperature extremes.Crossref | GoogleScholarGoogle Scholar |

Garcia-Cardeña G, Fan R, Shah V, Sorrentino R, Cirino G, Papapetropoulos A, Sessa WC (1998) Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 392, 821–824.
Dynamic activation of endothelial nitric oxide synthase by Hsp90.Crossref | GoogleScholarGoogle Scholar | 9580552PubMed |

Gerlach D (1972) ‘Zarys mikrotechniki botanicznej.’ (Państwowe Wydawnictwo Rolnicze i Leśne: Warszawa, Poland) [In Polish]

Halbrecq B, Rommedenne P, Ledent JF (2005) Evolution of flowering, ripening and seed set in buckwheat (Fagopyrum esculentum Moench.): quantitative analysis. European Journal of Agronomy 23, 209–224.
Evolution of flowering, ripening and seed set in buckwheat (Fagopyrum esculentum Moench.): quantitative analysis.Crossref | GoogleScholarGoogle Scholar |

Huang B, Xu C (2008) Identification and characterization of proteins associated with plant tolerance to heat stress. Journal of Integrative Plant Biology 50, 1230–1237.
Identification and characterization of proteins associated with plant tolerance to heat stress.Crossref | GoogleScholarGoogle Scholar | 19017110PubMed |

Huang R, Liu Z, Xing M, Yang Y, Wu X, Liu H, Liang W (2019) Heat stress suppresses Brassica napus seed oil accumulation by inhibition of photosynthesis and BnWRI1 pathway. Plant & Cell Physiology 60, 1457–1470.
Heat stress suppresses Brassica napus seed oil accumulation by inhibition of photosynthesis and BnWRI1 pathway.Crossref | GoogleScholarGoogle Scholar |

Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224–230.
Energy balance and acclimation to light and cold.Crossref | GoogleScholarGoogle Scholar |

Hura T, Hura K, Ostrowska A, Dziurka K (2015) Rapid plant rehydration initiates permanent and adverse changes in the photosynthetic apparatus of triticale. Plant and Soil 397, 127–145.
Rapid plant rehydration initiates permanent and adverse changes in the photosynthetic apparatus of triticale.Crossref | GoogleScholarGoogle Scholar |

Hura T, Hura K, Ostrowska A, Gadzinowska J, Grzesiak MT, Dziurka K, Dubas E (2018) Rieske iron-sulfur protein of cytochrome-b6f is involved in plant recovery after drought stress. Environmental and Experimental Botany 156, 228–239.
Rieske iron-sulfur protein of cytochrome-b6f is involved in plant recovery after drought stress.Crossref | GoogleScholarGoogle Scholar |

Hura T, Hura K, Ostrowska A, Gadzinowska J, Fiust A (2019) Water stress-induced flag leaf senescence may be accelerated by rehydration. Journal of Plant Physiology 236, 109–116.
Water stress-induced flag leaf senescence may be accelerated by rehydration.Crossref | GoogleScholarGoogle Scholar | 30947027PubMed |

Hüve K, Bichele I, Tobias M, Niinemets Ü (2006) Heat sensitivity of photosynthetic electron transport varies during the day due to changes in sugars and osmotic potential. Plant, Cell & Environment 29, 212–228.
Heat sensitivity of photosynthetic electron transport varies during the day due to changes in sugars and osmotic potential.Crossref | GoogleScholarGoogle Scholar |

Imai J, Yahara I (2000) Role of Hsp90 in salt stress tolerance via stabilization and regulation of calcineurin. Molecular and Cellular Biology 20, 9262–9270.
Role of Hsp90 in salt stress tolerance via stabilization and regulation of calcineurin.Crossref | GoogleScholarGoogle Scholar | 11094077PubMed |

Imai J, Maruya M, Yashiroda H, Yahara I, Tanaka K (2003) The molecular chaperone Hsp90 plays a role in the assembly and maintenance of the 26S proteasome. The EMBO Journal 22, 3557–3567.
The molecular chaperone Hsp90 plays a role in the assembly and maintenance of the 26S proteasome.Crossref | GoogleScholarGoogle Scholar | 12853471PubMed |

Kadrylova LR, Mukhametshina RR (2015) Pollen productivity and fertility of pollen in the genus Fagopyrum mill. Research Journal of Pharmaceutical, Biological and Chemical Sciences 6, 1695–1702.

Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dąbrowski A, et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynthesis Research 122, 121–158.
Frequently asked questions about in vivo chlorophyll fluorescence: practical issues.Crossref | GoogleScholarGoogle Scholar | 25119687PubMed |

Kurien BT, Scofield RH (2003) Protein blotting: a review. Journal of Immunological Methods 274, 1–15.
Protein blotting: a review.Crossref | GoogleScholarGoogle Scholar | 12609528PubMed |

Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 5432063PubMed |

Li H, Liu SS, Yi CY, Wang F, Zhou J, Xia XJ, Shi K, Zhou YH, Yu JQ (2014) Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants. Plant, Cell & Environment 37, 2768–2780.
Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants.Crossref | GoogleScholarGoogle Scholar |

Li H, Ahammed GJ, Zhou G, Xia X, Zhou J, Shi K, Yu J, Zhou Y (2016) Unraveling main limiting sites of photosynthesis under below- and above-ground heat stress in cucumber and the alleviatory role of luffa rootstock. Frontiers in Plant Science 7, 746.
Unraveling main limiting sites of photosynthesis under below- and above-ground heat stress in cucumber and the alleviatory role of luffa rootstock.Crossref | GoogleScholarGoogle Scholar | 27313587PubMed |

McGregor DI (1981) Pattern of flower and pod development in rapeseed. Canadian Journal of Plant Science 61, 275–282.
Pattern of flower and pod development in rapeseed.Crossref | GoogleScholarGoogle Scholar |

Melser C, Klinkhamer IPG (2001) Selective seed abortion increases offspring survival in Cynoglossum officinale (Boraginaceae). American Journal of Botany 88, 1033–1040.
Selective seed abortion increases offspring survival in Cynoglossum officinale (Boraginaceae).Crossref | GoogleScholarGoogle Scholar | 11410467PubMed |

Mihailova G, Petkova S, Buchel C, Georgieva K (2011) Desiccation of the resurrection plant Haberlea rhodopensis at high temperature. Photosynthesis Research 108, 5–13.
Desiccation of the resurrection plant Haberlea rhodopensis at high temperature.Crossref | GoogleScholarGoogle Scholar | 21399978PubMed |

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environment al stress. Biochimica et Biophysica Acta 1767, 414–421.
Photoinhibition of photosystem II under environment al stress.Crossref | GoogleScholarGoogle Scholar | 17207454PubMed |

Picard D, Khursheed B, Garabedian MJ, Fortin MG, Lindquist S, Yamamoto KR (1990) Reduced levels of Hsp90 compromise steroid receptor action in vivo. Nature 348, 166–168.
Reduced levels of Hsp90 compromise steroid receptor action in vivo.Crossref | GoogleScholarGoogle Scholar | 2234079PubMed |

Płażek A, Słomka A, Kopeć P, Dziurka M, Hornyák M, Sychta K, Pastuszak J, Dubert F (2019) Effects of high temperature on embryological development and hormone profile in flowers and leaves of common buckwheat (Fagopyrum esculentum Moench). International Journal of Molecular Sciences 20, 1705.
Effects of high temperature on embryological development and hormone profile in flowers and leaves of common buckwheat (Fagopyrum esculentum Moench).Crossref | GoogleScholarGoogle Scholar |

Polle A (1996) Mehler reaction: friend or foe in photosynthesis? Botanica Acta 109, 84–89.
Mehler reaction: friend or foe in photosynthesis?Crossref | GoogleScholarGoogle Scholar |

Richter K, Buchner J (2001) Hsp90: chaperoning signal transduction. Journal of Cellular Physiology 188, 281–290.
Hsp90: chaperoning signal transduction.Crossref | GoogleScholarGoogle Scholar | 11473354PubMed |

Rieu I, Twell D, Firon N (2017) Pollen development at high temperature: from acclimation to collapse. Plant Physiology 173, 1967–1976.
Pollen development at high temperature: from acclimation to collapse.Crossref | GoogleScholarGoogle Scholar | 28246296PubMed |

Sinsawat V, Leipner J, Stamp P, Fracheboud Y (2004) Effect of heat stress on photosynthetic apparatus in maize (Zea mays L.) grown at control or high temperature. Environmental and Experimental Botany 52, 123–129.
Effect of heat stress on photosynthetic apparatus in maize (Zea mays L.) grown at control or high temperature.Crossref | GoogleScholarGoogle Scholar |

Slawinska J, Obendorf RL (2001) Buckwheat seed set in planta and during in vitro inflorescence culture: evaluation of temperature and water deficit stress. Seed Science Research 11, 223–233.
Buckwheat seed set in planta and during in vitro inflorescence culture: evaluation of temperature and water deficit stress.Crossref | GoogleScholarGoogle Scholar |

Słomka A, Michno K, Dubert F, Dziurka M, Kopeć P, Płażek A (2017) Embryological background of low seed set in distylous common buckwheat (Fagopyrum esculentum Moench) with biased morph ratios, and biostimulant-induced improvement of it. Crop & Pasture Science 68, 680–690.
Embryological background of low seed set in distylous common buckwheat (Fagopyrum esculentum Moench) with biased morph ratios, and biostimulant-induced improvement of it.Crossref | GoogleScholarGoogle Scholar |

Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12, 253–279.
Flower and fruit abortion: proximate causes and ultimate functions.Crossref | GoogleScholarGoogle Scholar |

Strasser RJ, Tsimilli-Michael M (2001) Stress in plants, from daily rhythm to global changes, detected and quantified by the JIP-Test. Chimie Nouvelle 75, 3321–3326.

Strasser RJ, Srivatava A, Tsimilli-Michael M (2000) The fluorescence transients as a tool to characterize and screen photosynthetic samples. In ‘Probing photosynthesis: mechanism, regulation and adaptation’. (Eds M Yunus, U Pathre, P Mohanty) pp. 45–483. (Taylor & Francis: Bristol, UK)

Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends in Plant Science 13, 178–182.
How do environmental stresses accelerate photoinhibition?Crossref | GoogleScholarGoogle Scholar | 18328775PubMed |

Takahashi M, Shiraishi T, Asada K (1988) Superoxide production in aprotic interior of chloroplast thylakoids. Archives of Biochemistry and Biophysics 267, 714–722.
Superoxide production in aprotic interior of chloroplast thylakoids.Crossref | GoogleScholarGoogle Scholar | 2850770PubMed |

Taylor DP, Obendorf RL (2001) Quantitative assessment of some factors limiting seed set in buckwheat. Crop Science 41, 1792–1799.
Quantitative assessment of some factors limiting seed set in buckwheat.Crossref | GoogleScholarGoogle Scholar |

Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and applications. Proceedings of the National Academy of Sciences of the United States of America 76, 4350–4354.
Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and applications.Crossref | GoogleScholarGoogle Scholar | 388439PubMed |

van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research 25, 147–150.
The use of chlorophyll fluorescence nomenclature in plant stress physiology.Crossref | GoogleScholarGoogle Scholar | 24420345PubMed |

Wang Y, Scarth R, Campbell C (2005) Interspecific hybridization between diploid Fagopyrum esculentum and tetraploid F. homotropicum. Canadian Journal of Plant Science 85, 41–48.
Interspecific hybridization between diploid Fagopyrum esculentum and tetraploid F. homotropicum.Crossref | GoogleScholarGoogle Scholar |

Wiese C, Shi LB, Heber U (1998) Oxygen reduction in the Mehler reaction is insufficient to protect photosystems I and II of leaves against photoinactivation. Physiologia Plantarum 102, 437–446.
Oxygen reduction in the Mehler reaction is insufficient to protect photosystems I and II of leaves against photoinactivation.Crossref | GoogleScholarGoogle Scholar |

Yan K, Chen P, Shao HB, Zhao SJ (2013) Characterization of photosynthetic electron transport chain in bioenergy crop Jerusalem artichoke (Helianthus tuberosus L.) under heat stress for sustainable cultivation. Industrial Crops and Products 50, 809–815.
Characterization of photosynthetic electron transport chain in bioenergy crop Jerusalem artichoke (Helianthus tuberosus L.) under heat stress for sustainable cultivation.Crossref | GoogleScholarGoogle Scholar |