A reversible light- and genotype-dependent acquired thermotolerance response protects the potato plant from damage due to excessive temperature
A powerful acquired thermotolerance response in potato was demonstrated and characterised in detail, showing the time course required for tolerance, the reversibility of the process and requirement for light.
Potato is particularly vulnerable to increased temperature, considered to be the most important uncontrollable factor affecting growth and yield of this globally significant crop. Here, we describe an acquired thermotolerance response in potato, whereby treatment at a mildly elevated temperature primes the plant for more severe heat stress. We define the time course for acquiring thermotolerance and demonstrate that light is essential for the process. In all four commercial tetraploid cultivars that were tested, acquisition of thermotolerance by priming was required for tolerance at elevated temperature. Accessions from several wild-type species and diploid genotypes did not require priming for heat tolerance under the test conditions employed, suggesting that useful variation for this trait exists. Physiological, transcriptomic and metabolomic approaches were employed to elucidate potential mechanisms that underpin the acquisition of heat tolerance. This analysis indicated a role for cell wall modification, auxin and ethylene signalling, and chromatin remodelling in acclimatory priming resulting in reduced metabolic perturbation and delayed stress responses in acclimated plants following transfer to 40 °C.
KeywordsAcquired thermotolerance Electrolyte leakage Heat tolerance Potato Redox couples Yield
Heat shock protein
Reactive oxygen species
This work was funded by the BBSRC Grant (BB/M004899/1) as part of the ERA-CAPS project HotSol, a Marie Skłodowska-Curie Individual Fellowship (Project number 702121 (ACQUIRE) to ECB) (H2020 Excellent Science) and the Scottish Government Rural and Environment Science and Analytical Services Division as part of the Strategic Research Programme 2016–2021.
- de Wit M, Galvão VC, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol 67:513–537. https://doi.org/10.1146/annurev-arplant-043015-112252 CrossRefPubMedGoogle Scholar
- Ducreux LJ, Morris WL, Prosser IM, Morris JA, Beale MH, Wright F, Shepherd T, Bryan GJ, Hedley PE, Taylor MA (2008) Expression profiling of potato germplasm differentiated in quality traits leads to the identification of candidate flavour and texture genes. J Exp Bot 59:4219–4231. https://doi.org/10.1093/jxb/ern264 CrossRefPubMedPubMedCentralGoogle Scholar
- Guy C (1999) The influence of temperature extremes on gene expression, genomic structure, and the evolution of induced tolerance in plants. In: Lerner HR (ed) Plant responses to environmental stresses. Marcel Dekker, New York, pp 497–548Google Scholar
- Hancock RD, Morris WL, Ducreux LJ, Morris JA, Usman M, Verrall SR, Fuller J, Simpson CG, Zhang R, Hedley PE, Taylor MA (2014) Physiological, biochemical and molecular responses of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ 37:439–450. https://doi.org/10.1111/pce.12168 CrossRefPubMedGoogle Scholar
- McLoughlin F, Basha E, Fowler ME, Kim M, Bordowitz J, Katiyar-Agarwal S, Vierling E (2016) Class I and II small heat shock proteins together with HSP101 protect protein translation factors during heat stress. Plant Physiol 172:1221–1236. https://doi.org/10.1104/pp.16.00536 PubMedPubMedCentralGoogle Scholar
- Morris WL, Hancock RD, Ducreux LJ, Morris JA, Usman M, Verrall SR, Sharma SK, Bryan G, McNicol JW, Hedley PE, Taylor MA (2014) Day length dependent restructuring of the leaf transcriptome and metabolome in potato genotypes with contrasting tuberization phenotypes. Plant Cell Environ 37:1351–1363. https://doi.org/10.1111/pce.12238 CrossRefPubMedGoogle Scholar
- Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
- Pornsiriwong W, Estavillo GM, Chan KX, Tee EE, Ganguly D, Crisp PA, Phua SY, Zhao C, Qiu J, Park J, Yong MT (2017) A chloroplast retrograde signal, 3′-phosphoadenosine 5′-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. ELife 21:6. https://doi.org/10.7554/eLife.23361 Google Scholar
- Prashar A, Hornyik C, Young V, McLean K, Sharma SK, Dale MF, Bryan GJ (2014) Construction of a dense SNP map of a highly heterozygous diploid potato population and QTL analysis of tuber shape and eye depth. Theor Appl Genet 127:2159–2171. https://doi.org/10.1007/s00122-014-2369-9 CrossRefPubMedGoogle Scholar
- Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939. https://doi.org/10.1111/j.1365-313X.2004.02016.x CrossRefPubMedGoogle Scholar
- Trapero-Mozos A, Morris WL, Ducreux LJ, McLean K, Stephens J, Torrance L, Bryan GJ, Hancock RD, Taylor MA (2017) Engineering heat tolerance in potato by temperature-dependent expression of a specific allele of HEAT SHOCK COGNATE 70. Plant Biotechnol J. https://doi.org/10.1111/pbi.12760 PubMedPubMedCentralGoogle Scholar
- Usadel B, Nagel A, Steinhauser D, Gibon Y, Bläsing OE, Redestig H, Sreenivasulu N, Krall L, Hannah MA, Poree F, Fernie AR (2006) PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinform 7:535. https://doi.org/10.1186/1471-2105-7-535 CrossRefGoogle Scholar
- Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Biol 42:579–620. https://doi.org/10.1146/annurev.pp.42.060191.003051 CrossRefGoogle Scholar