Potato (Solanum tuberosum) is highly water and space efficient but susceptible to abiotic stresses such as heat, drought, and flooding, which are severely exacerbated by climate change. Our understanding of crop acclimation to abiotic stress, however, remains limited. Here, we present a comprehensive molecular and physiological high-throughput profiling of potato (Solanum tuberosum, cv. Désirée) under heat, drought, and waterlogging applied as single stresses or in combinations designed to mimic realistic future scenarios. Stress responses were monitored via daily phenotyping and multi-omics analyses of leaf samples comprising proteomics, targeted transcriptomics, metabolomics, and hormonomics at several timepoints during and after stress treatments. Additionally, critical metabolites of tuber samples were analyzed at the end of the stress period. We performed integrative multi-omics data analysis using a bioinformatic pipeline that we established based on machine learning and knowledge networks. Waterlogging produced the most immediate and dramatic effects on potato plants, interestingly activating ABA responses similar to drought stress. In addition, we observed distinct stress signatures at multiple molecular levels in response to heat or drought and to a combination of both. In response to all treatments, we found a downregulation of photosynthesis at different molecular levels, an accumulation of minor amino acids, and diverse stress-induced hormones. Our integrative multi-omics analysis provides global insights into plant stress responses, facilitating improved breeding strategies toward climate-adapted potato varieties.

Department Biologie Lehrstuhl für Biochemie Friedrich Alexander Universität Erlangen Nürnberg Staudstr 5 91058 Erlangen Germany

Department of Biosciences Durham University South Road Durham DH1 3LE UK

Department of Biotechnology and Systems Biology National Institute of Biology Večna pot 121 1000 Ljubljana Slovenia

Department of Functional and Evolutionary Ecology Molecular Systems Biology University Vienna Djerassiplatz 1 1030 Vienna Austria

Laboratory of Growth Regulators Palacký University in Olomouc and Institute of Experimental Botany AS CR Šlechtitelů 27 Olomouc 779 00 Czech Republic

Mass Spectrometry Unit Research Support Facilities Faculty of Life Sciences University Vienna Djerassiplatz 1 1030 Vienna Austria

Plant Stress Resilience Institute of Environmental Biology Utrecht University Heidelberglaan 8 3584 CS Utrecht The Netherlands

PSI spol s r o Prumyslova 470 CZ 664 24 Drásov Czech Republic

School for Viticulture and Enology University of Nova Gorica Gladni trg 8 5271 Vipava Slovenia

Vienna Metabolomics Center University Vienna Djerassiplatz 1 1030 Vienna Austria

Wageningen University and Research Department of Plant Breeding Droevendaalsesteeg 1 6708 PB Wageningen The Netherlands

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Abdelhakim  LOA, Palma  CFF, Zhou  R, Wollenweber  B, Ottosen  CO, Rosenqvist  E. The effect of individual and combined drought and heat stress under elevated CO2 on physiological responses in spring wheat genotypes. Plant Physiol Biochem. 2021a:162:301–314. 10.1016/j.plaphy.2021.02.015 PubMed DOI

Abdelhakim  LOA, Pleskacová  B, Rodriguez-Granados  NY, Sasidharan  R, Perez-Borroto  LS, Sonnewald  S, Gruden  K, Vothknecht  UC, Teige  M, Panzarová  K. High throughput image-based phenotyping for determining morphological and physiological responses to single and combined stresses in potato. J Vis Exp. 2024:208:e66255. 10.3791/66255 PubMed DOI

Abdelhakim  LOA, Rosenqvist  E, Wollenweber  B, Spyroglou  I, Ottosen  C-O, Panzarová  K. Investigating combined drought- and heat stress effects in wheat under controlled conditions by dynamic image-based phenotyping. Agronomy. 2021b:11(2):364. 10.3390/agronomy11020364 DOI

Abelenda  JA, Bergonzi  S, Oortwijn  M, Sonnewald  S, Du  M, Visser  RGF, Sonnewald  U, Bachem  CWB. Source-sink regulation is mediated by interaction of an FT homolog with a SWEET protein in potato. Curr Biol. 2019:29(7):1178–1186.e6. 10.1016/j.cub.2019.02.018 PubMed DOI

Abelenda  JA, Cruz-Oró  E, Franco-Zorrilla  JM, Prat  S. Potato StCONSTANS-like1 suppresses storage organ formation by directly activating the FT-like StSP5G repressor. Curr Biol. 2016:26(7):872–881. 10.1016/j.cub.2016.01.066 PubMed DOI

Akbudak  MA, Yildiz  S, Filiz  E. Pathogenesis related protein-1 (PR-1) genes in tomato (Solanum lycopersicum L.): bioinformatics analyses and expression profiles in response to drought stress. Genomics. 2020:112(6):4089–4099. 10.1016/j.ygeno.2020.07.004 PubMed DOI

Awlia  M, Nigro  A, Fajkus  J, Schmoeckel  SM, Negrão  S, Santelia  D, Trtílek  M, Tester  M, Julkowska  MM, Panzarová  K. High-throughput non-destructive phenotyping of traits that contribute to salinity tolerance in Arabidopsis thaliana. Front Plant Sci. 2016:7:1414. 10.3389/fpls.2016.01414 PubMed DOI PMC

Bachmann  A, Hause  B, Maucher  H, Garbe  E, Vörös  K, Weichert  H, Wasternack  C, Feussner  I. Jasmonate-induced lipid peroxidation in barley leaves initiated by distinct 13-LOX forms of chloroplasts. Biol Chem. 2002:383(10):1645–1657. 10.1515/BC.2002.185 PubMed DOI

Baebler  Š, Svalina  M, Petek  M, Stare  K, Rotter  A, Pompe-Novak  M, Gruden  K. quantGenius: implementation of a decision support system for qPCR-based gene quantification. BMC Bioinformatics. 2017:18(1):276. 10.1186/s12859-017-1688-7 PubMed DOI PMC

Bailey-Serres  J, Parker  JE, Ainsworth  EA, Oldroyd  GED, Schroeder  JI. Genetic strategies for improving crop yields. Nature. 2019:575(7781):109–118. 10.1038/s41586-019-1679-0 PubMed DOI PMC

Balfagón  D, Sengupta  S, Gómez-Cadenas  A, Fritschi  FB, Azad  RK, Mittler  R, Zandalinas  SI. Jasmonic acid is required for plant acclimation to a combination of high light and heat stress. Plant Physiol. 2019:181(4):1668–1682. 10.1104/pp.19.00956 PubMed DOI PMC

Benitez-Alfonso  Y, Soanes  BK, Zimba  S, Sinanaj  B, German  L, Sharma  V, Bohra  A, Kolesnikova  A, Dunn  JA, Martin  AC, et al.  Enhancing climate change resilience in agricultural crops. Curr Biol. 2023:33(23):R1246–R1261. 10.1016/j.cub.2023.10.028 PubMed DOI

Bittner  A, Cieśla  A, Gruden  K, Lukan  T, Mahmud  S, Teige  M, Vothknecht  UC, Wurzinger  B. Organelles and phytohormones: a network of interactions in plant stress responses. J Exp Bot. 2022:73(21):7165–7181. 10.1093/jxb/erac384 PubMed DOI PMC

Bleker  C, Ramšak  Ž, Bittner  A, Podpečan  V, Zagorščak  M, Wurzinger  B, Baebler  Š, Petek  M, Križnik  M, van Dieren  A, et al.  Stress knowledge map: a knowledge graph resource for systems biology analysis of plant stress responses. Plant Commun. 2024:5(6):100920. 10.1016/j.xplc.2024.100920 PubMed DOI PMC

Cembrowska-Lech  D, Krzeminska  A, Miller  T, Nowakowska  A, Adamski  C, Radaczynska  M, Mikiciuk  G, Mikiciuk  M. An integrated multi-omics and artificial intelligence framework for advance plant phenotyping in horticulture. Biology (Basel). 2023:12(10):1298. 10.3390/biology12101298 PubMed DOI PMC

Chaturvedi  P, Doerfler  H, Jegadeesan  S, Ghatak  A, Pressman  E, Castillejo  MA, Wienkoop  S, Egelhofer  V, Firon  N, Weckwerth  W. Heat-treatment-responsive proteins in different developmental stages of tomato pollen detected by targeted mass accuracy precursor alignment (tMAPA). J Proteome Res. 2015:14(11):4463–4471. 10.1021/pr501240n PubMed DOI

Chaturvedi  P, Ischebeck  T, Egelhofer  V, Lichtscheidl  I, Weckwerth  W. Cell-specific analysis of the tomato pollen proteome from pollen mother cell to mature pollen provides evidence for developmental priming. J Proteome Res. 2013:12(11):4892–4903. 10.1021/pr400197p PubMed DOI

Chen  Q, Hu  T, Li  X, Song  CP, Zhu  JK, Chen  L, Zhao  Y. Phosphorylation of SWEET sucrose transporters regulates plant root:shoot ratio under drought. Nat Plants. 2022:8(1):68–77. 10.1038/s41477-021-01040-7 PubMed DOI

Clarke  SM, Cristescu  SM, Miersch  O, Harren  FJM, Wasternack  C, Mur  LAJ. Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol. 2009:182(1):175–187. 10.1111/j.1469-8137.2008.02735.x PubMed DOI

Cutler  SR, Rodriguez  PL, Finkelstein  RR, Abrams  SR. Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol. 2010:61:651–679. 10.1146/annurev-arplant-042809-112122 PubMed DOI

Dahal  K, Li  XQ, Tai  H, Creelman  A, Bizimungu  B. Improving potato stress tolerance and tuber yield under a climate change scenario—a current overview. Front Plant Sci. 2019:10:563. 10.3389/fpls.2019.00563 PubMed DOI PMC

Demirel  U, Morris  WL, Ducreux  LJM, Yavuz  C, Asim  A, Tindas  I, Campbell  R, Morris  JA, Verrall  SR, Hedley  PE, et al.  Physiological, biochemical, and transcriptional responses to single and combined abiotic stress in stress-tolerant and stress-sensitive potato genotypes. Front Plant Sci. 2020:11:169. 10.3389/fpls.2020.00169 PubMed DOI PMC

FAO . The impact of disasters on agriculture and food security 2023—avoiding and reducing losses through investment in resilience. Rome, Italy: FAO; 2023. p. #168.

Findurová  H, Veselá  B, Panzarová  K, Pytela  J, Trtílek  M, Klem  K. Phenotyping drought tolerance and yield performance of barley using a combination of imaging methods. Environ Exp Bot. 2023:209:105314. 10.1016/j.envexpbot.2023.105314 DOI

Floková  K, Tarkowská  D, Miersch  O, Strnad  M, Wasternack  C, Novák  O. UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry. 2014:105:147–157. 10.1016/j.phytochem.2014.05.015 PubMed DOI

Gautam  T, Dutta  M, Jaiswal  V, Zinta  G, Gahlaut  V, Kumar  S. Emerging roles of SWEET sugar transporters in plant development and abiotic stress responses. Cells. 2022:11(8):1303. 10.3390/cells11081303 PubMed DOI PMC

Geldhof  B, Pattyn  J, Van de Poel  B. From a different angle: genetic diversity underlies differentiation of waterlogging-induced epinasty in tomato. Front Plant Sci. 2023:14:1178778. 10.3389/fpls.2023.1178778 PubMed DOI PMC

Ghatak  A, Chaturvedi  P, Bachmann  G, Valledor  L, Ramšak  Ž, Bazargani  MM, Bajaj  P, Jegadeesan  S, Li  W, Sun  X, et al.  Physiological and proteomic signatures reveal mechanisms of superior drought resilience in pearl millet compared to wheat. Front Plant Sci. 2020:11:600278. 10.3389/fpls.2020.600278 PubMed DOI PMC

Ghatak  A, Chaturvedi  P, Nagler  M, Roustan  V, Lyon  D, Bachmann  G, Postl  W, Schröfl  A, Desai  N, Varshney  RK, et al.  Comprehensive tissue-specific proteome analysis of drought stress responses in Pennisetum glaucum (L.) R. Br. (Pearl millet). J Proteomics. 2016:143:122–135. 10.1016/j.jprot.2016.02.032 PubMed DOI

Grieco  M, Roustan  V, Dermendjiev  G, Rantala  S, Jain  A, Leonardelli  M, Neumann  K, Berger  V, Engelmeier  D, Bachmann  G, et al.  Adjustment of photosynthetic activity to drought and fluctuating light in wheat. Plant Cell Environ. 2020:43(6):1484–1500. 10.1111/pce.13756 PubMed DOI PMC

Guihur  A, Rebeaud  ME, Goloubinoff  P. How do plants feel the heat and survive?  Trends Biochem Sci. 2022:47(10):824–838. 10.1016/j.tibs.2022.05.004 PubMed DOI

Hall  RD, D'Auria  JC, Silva Ferreira  AC, Gibon  Y, Kruszka  D, Mishra  P, van de Zedde  R. High-throughput plant phenotyping: a role for metabolomics?  Trends Plant Sci. 2022:27(6):549–563. 10.1016/j.tplants.2022.02.001 PubMed DOI

Hancock  RD, Morris  WL, Ducreux  LJ, Morris  JA, Usman  M, Verrall  SR, Fuller  J, Simpson  CG, Zhang  R, Hedley  PE, et al.  Physiological, biochemical and molecular responses of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ. 2014:37(2):439–450. 10.1111/pce.12168 PubMed DOI

Hastilestari  BR, Lorenz  J, Reid  S, Hofmann  J, Pscheidt  D, Sonnewald  U, Sonnewald  S. Deciphering source and sink responses of potato plants (Solanum tuberosum L.) to elevated temperatures. Plant Cell Environ. 2018:41(11):2600–2616. 10.1111/pce.13366 PubMed DOI

Hoehenwarter  W, van Dongen  JT, Wienkoop  S, Steinfath  M, Hummel  J, Erban  A, Sulpice  R, Regierer  B, Kopka  J, Geigenberger  P, et al.  A rapid approach for phenotype-screening and database independent detection of cSNP/protein polymorphism using mass accuracy precursor alignment. Proteomics. 2008:8(20):4214–4225. 10.1002/pmic.200701047 PubMed DOI

Jackson  MB, Campbell  DJ. Waterlogging and petiole epinasty in tomato: the role of ethylene and low oxygen. New Phytol. 1976:76(1):21–29. 10.1111/j.1469-8137.1976.tb01434.x DOI

Jackson  MB, Hall  KC. Early stomatal closure in waterlogged pea plants is mediated by abscisic acid in the absence of foliar water deficits. Plant Cell Environ. 1987:10(2):121–130. 10.1111/1365-3040.ep11602085 DOI

Jamil  IN, Remali  J, Azizan  KA, Nor Muhammad  NA, Arita  M, Goh  HH, Aizat  WM. Systematic multi-omics integration (MOI) approach in plant systems biology. Front Plant Sci. 2020:11:944. 10.3389/fpls.2020.00944 PubMed DOI PMC

Joshi  S, Patil  S, Shaikh  A, Jamla  M, Kumar  V. Modern omics toolbox for producing combined and multifactorial abiotic stress tolerant plants. Plant Stress. 2024:11:100301. 10.1016/j.stress.2023.100301 DOI

Jovović  Z, Broćić  Z, Velimirović  A, Dolijanović  Ž, Komnenić  A. The influence of flooding on the main parameters of potato productivity. In: VIII South-Eastern Europe symposium on vegetables and potatoes 1320. Leuven, Belgium: International Society for Horticultural Science (ISHS); 2021. p. 133–138.

Kanehisa  M, Furumichi  M, Tanabe  M, Sato  Y, Morishima  K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017:45(D1):D353–D361. 10.1093/nar/gkw1092 PubMed DOI PMC

Koch  L, Lehretz  GG, Sonnewald  U, Sonnewald  S. Yield reduction caused by elevated temperatures and high nitrogen fertilization is mitigated by SP6A overexpression in potato (Solanum tuberosum L.). Plant J. 2024:117(6):1702–1715. 10.1111/tpj.16679 PubMed DOI

Kohl  M. MKinfer: inferential statistics. R package version 1.2. 2024. https://github.com/stamats/MKinfer.

Kromdijk  J, Głowacka  K, Leonelli  L, Gabilly  ST, Iwai  M, Niyogi  KK, Long  SP. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science. 2016:354(6314):857–861. 10.1126/science.aai8878 PubMed DOI

Kuhn  M. Building predictive models in R using the caret package. J Statist Soft. 2008:28(5):1–26. 10.18637/jss.v028.i05 DOI

Lal  MK, Tiwari  RK, Kumar  A, Dey  A, Kumar  R, Kumar  D, Jaiswal  A, Changan  SS, Raigond  P, Dutt  S, et al.  Mechanistic concept of physiological, biochemical, and molecular responses of the potato crop to heat and drought stress. Plants (Basel). 2022:11(21):2857. 10.3390/plants11212857 PubMed DOI PMC

Lee  AH, Shannon  CP, Amenyogbe  N, Bennike  TB, Diray-Arce  J, Idoko  OT, Gill  EE, Ben-Othman  R, Pomat  WS, van Haren  SD, et al.  Dynamic molecular changes during the first week of human life follow a robust developmental trajectory. Nat Commun. 2019:10(1):1092. 10.1038/s41467-019-08794-x PubMed DOI PMC

Leeggangers  HACF, Rodriguez-Granados  NY, Macias-Honti  MG, Sasidharan  R. A helping hand when drowning: the versatile role of ethylene in root flooding resilience. Environ Exp Bot. 2023:213:105422. 10.1016/j.envexpbot.2023.105422 DOI

Lehretz  GG, Sonnewald  S, Lugassi  N, Granot  D, Sonnewald  U. Future-proofing potato for drought and heat tolerance by overexpression of hexokinase and SP6A. Front Plant Sci. 2020:11:614534. 10.3389/fpls.2020.614534 PubMed DOI PMC

Li  B, Zeng  Y, Cao  W, Zhang  W, Cheng  L, Yin  H, Wu  Q, Wang  X, Huang  Y, Lau  WCY, et al.  A distinct giant coat protein complex II vesicle population in Arabidopsis thaliana. Nat Plants. 2021:7(10):1335–1346. 10.1038/s41477-021-00997-9 PubMed DOI

Liu  T, Salguero  P, Petek  M, Martinez-Mira  C, Balzano-Nogueira  L, Ramšak  Ž, McIntyre  L, Gruden  K, Tarazona  S, Conesa  A. PaintOmics 4: new tools for the integrative analysis of multi-omics datasets supported by multiple pathway databases. Nucleic Acids Res. 2022:50(W1):W551–W559. 10.1093/nar/gkac352 PubMed DOI PMC

Lothier  J, Diab  H, Cukier  C, Limami  AM, Tcherkez  G. Metabolic responses to waterlogging differ between roots and shoots and reflect phloem transport alteration in Medicago truncatula. Plants (Basel). 2020:9(10):1373. 10.3390/plants9101373 PubMed DOI PMC

Lozano-Elena  F, Fàbregas  N, Coleto-Alcudia  V, Caño-Delgado  AI. Analysis of metabolic dynamics during drought stress in Arabidopsis plants. Sci Data. 2022:9(1):90. 10.1038/s41597-022-01161-4 PubMed DOI PMC

Lozano-Juste  J, Cutler  SR. Hormone signalling: ABA has a breakdown. Nat Plants. 2016:2(9):16137. 10.1038/nplants.2016.137 PubMed DOI

Lundberg  SM, Lee  S-I. A unified approach to interpreting model predictions. In: Proceedings of the 31st international conference on neural information processing systems. Long Beach, California, USA: Curran Associates Inc.; 2017. p. 4768–4777.

Mahmud  S, Ullah  C, Kortz  A, Bhattacharyya  S, Yu  P, Gershenzon  J, Vothknecht  UC. Constitutive expression of JASMONATE RESISTANT 1 induces molecular changes that prime the plants to better withstand drought. Plant Cell Environ. 2022:45(10):2906–2922. 10.1111/pce.14402 PubMed DOI

Manjunath  KK, Krishna  H, Devate  NB, Sunilkumar  VP, Patil  SP, Chauhan  D, Singh  S, Kumar  S, Jain  N, Singh  GP, et al.  QTL mapping: insights into genomic regions governing component traits of yield under combined heat and drought stress in wheat. Front Genet. 2023:14:1282240. 10.3389/fgene.2023.1282240 PubMed DOI PMC

Mathur  S, Agrawal  D, Jajoo  A. Photosynthesis: response to high temperature stress. J Photochem Photobiol B. 2014:137:116–126. 10.1016/j.jphotobiol.2014.01.010 PubMed DOI

Mishra  S, Srivastava  AK, Khan  AW, Tran  LP, Nguyen  HT. The era of panomics-driven gene discovery in plants. Trends Plant Sci. 2024:29(9):995–1005. 10.1016/j.tplants.2024.03.007 PubMed DOI

Mittler  R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006:11(1):15–19. 10.1016/j.tplants.2005.11.002 PubMed DOI

Nakamura  Y, Mithöfer  A, Kombrink  E, Boland  W, Hamamoto  S, Uozumi  N, Tohma  K, Ueda  M. 12-hydroxyjasmonic acid glucoside is a COI1-JAZ-independent activator of leaf-closing movement in Samanea saman. Plant Physiol. 2011:155(3):1226–1236. 10.1104/pp.110.168617 PubMed DOI PMC

Navarro  C, Abelenda  JA, Cruz-Oró  E, Cuéllar  CA, Tamaki  S, Silva  J, Shimamoto  K, Prat  S. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature. 2011:478(7367):119–122. 10.1038/nature10431 PubMed DOI

Núñez-Lillo  G, Ponce  E, Arancibia-Guerra  C, Carpentier  S, Carrasco-Pancorbo  A, Olmo-García  L, Chirinos  R, Campos  D, Campos-Vargas  R, Meneses  C, et al.  A multiomics integrative analysis of color de-synchronization with softening of ‘hass’ avocado fruit: a first insight into a complex physiological disorder. Food Chem. 2023:408:135215. 10.1016/j.foodchem.2022.135215 PubMed DOI

Núñez-Lillo  G, Ponce  E, Beyer  CP, Álvaro  JE, Meneses  C, Pedreschi  R. A first omics data integration approach in hass avocados to evaluate rootstock–scion interactions: from aerial and root plant growth to fruit development. Plants (Basel). 2024:13(5):603. 10.3390/plants13050603 PubMed DOI PMC

Obata  T, Klemens  PAW, Rosado-Souza  L, Schlereth  A, Gisel  A, Stavolone  L, Zierer  W, Morales  N, Mueller  LA, Zeeman  SC, et al.  Metabolic profiles of six African cultivars of cassava (Manihot esculenta crantz) highlight bottlenecks of root yield. Plant J. 2020:102(6):1202–1219. 10.1111/tpj.14693 PubMed DOI

Oksanen  J, Simpson  G, Blanchet  F, Kindt  R, Legendre  P, Minchin  P, Hara  O, Solymos  R, Stevens  P, Szöcs  H, et al.  vegan: Community Ecology Package. R package version 2.6-2. 2022. https://github.com/vegandevs/vegan, https://vegandevs.github.io/vegan/

Paoletti  AC, Parmely  TJ, Tomomori-Sato  C, Sato  S, Zhu  D, Conaway  RC, Conaway  JW, Florens  L, Washburn  MP. Quantitative proteomic analysis of distinct mammalian mediator complexes using normalized spectral abundance factors. Proc Natl Acad Sci U S A. 2006:103(50):18928–18933. 10.1073/pnas.0606379103 PubMed DOI PMC

Park  JS, Park  SJ, Kwon  SY, Shin  AY, Moon  KB, Park  JM, Cho  HS, Park  SU, Jeon  JH, Kim  HS, et al.  Temporally distinct regulatory pathways coordinate thermo-responsive storage organ formation in potato. Cell Rep. 2022:38(13):110579. 10.1016/j.celrep.2022.110579 PubMed DOI

Petek  M, Rotter  A, Kogovšek  P, Baebler  S, Mithöfer  A, Gruden  K. Potato virus Y infection hinders potato defence response and renders plants more vulnerable to Colorado potato beetle attack. Mol Ecol. 2014:23(21):5378–5391. 10.1111/mec.12932 PubMed DOI PMC

Petek  M, Zagorščak  M, Ramšak  Ž, Sanders  S, Tomaž  Š, Tseng  E, Zouine  M, Coll  A, Gruden  K. Cultivar-specific transcriptome and pan-transcriptome reconstruction of tetraploid potato. Sci Data. 2020:7(1):249. 10.1038/s41597-020-00581-4 PubMed DOI PMC

Ployet  R, Veneziano Labate  MT, Regiani Cataldi  T, Christina  M, Morel  M, San Clemente  H, Denis  M, Favreau  B, Tomazello Filho  M, Laclau  J-P, et al.  A systems biology view of wood formation in Eucalyptus grandis trees submitted to different potassium and water regimes. New Phytol. 2019:223(2):766–782. 10.1111/nph.15802 PubMed DOI

Quint  M, Delker  C, Franklin  KA, Wigge  PA, Halliday  KJ, van Zanten  M. Molecular and genetic control of plant thermomorphogenesis. Nat Plants. 2016:2(1):15190. 10.1038/nplants.2015.190 PubMed DOI

Renziehausen  T, Frings  S, Schmidt-Schippers  R. ‘Against all floods’: plant adaptation to flooding stress and combined abiotic stresses. Plant J. 2024:117(6):1836–1855. 10.1111/tpj.16614 PubMed DOI

Rivero  RM, Mittler  R, Blumwald  E, Zandalinas  SI. Developing climate-resilient crops: improving plant tolerance to stress combination. Plant J. 2022:109(2):373–389. 10.1111/tpj.15483 PubMed DOI

Rohart  F, Gautier  B, Singh  A, Lê Cao  KA. mixOmics: an R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol. 2017:13(11):e1005752. 10.1371/journal.pcbi.1005752 PubMed DOI PMC

Sato  H, Mizoi  J, Shinozaki  K, Yamaguchi-Shinozaki  K. Complex plant responses to drought and heat stress under climate change. Plant J. 2024:117(6):1873–1892. 10.1111/tpj.16612 PubMed DOI

Sauter  M. Root responses to flooding. Curr Opin Plant Biol. 2013:16(3):282–286. 10.1016/j.pbi.2013.03.013 PubMed DOI

Shannon  P, Markiel  A, Ozier  O, Baliga  NS, Wang  JT, Ramage  D, Amin  N, Schwikowski  B, Ideker  T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003:13:2498–2504. PubMed PMC

Singh  A, Shannon  CP, Gautier  B, Rohart  F, Vacher  M, Tebbutt  SJ, Lê Cao  KA. DIABLO: an integrative approach for identifying key molecular drivers from multi-omics assays. Bioinformatics. 2019:35(17):3055–3062. 10.1093/bioinformatics/bty1054 PubMed DOI PMC

Sinha  R, Peláez-Vico  MA, Shostak  B, Nguyen  TT, Pascual  LS, Ogden  AM, Lyu  Z, Zandalinas  SI, Joshi  T, Fritschi  FB, et al.  The effects of multifactorial stress combination on rice and maize. Plant Physiol. 2024:194(3):1358–1369. 10.1093/plphys/kiad557 PubMed DOI

Široká  J, Brunoni  F, Pěnčík  A, Mik  V, Žukauskaitė  A, Strnad  M, Novák  O, Floková  K. High-throughput interspecies profiling of acidic plant hormones using miniaturised sample processing. Plant Methods. 2022:18(1):122. 10.1186/s13007-022-00954-3 PubMed DOI PMC

Smith  AM, Zeeman  SC. Quantification of starch in plant tissues. Nat Protoc. 2006:1(3):1342–1345. 10.1038/nprot.2006.232 PubMed DOI

Stael  S, Kmiecik  P, Willems  P, Van Der Kelen  K, Coll  NS, Teige  M, Van Breusegem  F. Plant innate immunity–sunny side up?  Trends Plant Sci. 2015:20(1):3–11. 10.1016/j.tplants.2014.10.002 PubMed DOI PMC

Subramanian  A, Tamayo  P, Mootha  VK, Mukherjee  S, Ebert  BL, Gillette  MA, Paulovich  A, Pomeroy  SL, Golub  TR, Lander  ES, et al.  Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005:102:15545–15550. 10.1073/pnas.0506580102 PubMed DOI PMC

Tang  R, Niu  S, Zhang  G, Chen  G, Haroon  M, Yang  Q, Rajora  OP, Li  X-Q. Physiological and growth responses of potato cultivars to heat stress. Botany. 2018:96(12):897–912. 10.1139/cjb-2018-0125 DOI

Trapero-Mozos  A, Morris  WL, Ducreux  LJM, McLean  K, Stephens  J, Torrance  L, Bryan  GJ, Hancock  RD, Taylor  MA. Engineering heat tolerance in potato by temperature-dependent expression of a specific allele of HEAT-SHOCK COGNATE 70. Plant Biotechnol J. 2018:16(1):197–207. 10.1111/pbi.12760 PubMed DOI PMC

von Gehren  P, Bomers  S, Tripolt  T, Söllinger  J, Prat  N, Redondo  B, Vorss  R, Teige  M, Kamptner  A, Ribarits  A. Farmers feel the climate change: variety choice as an adaptation strategy of European potato farmers. Climate. 2023:11(9):189. 10.3390/cli11090189 DOI

Wasternack  C, Feussner  I. The oxylipin pathways: biochemistry and function. Annu Rev Plant Biol. 2018:69(1):363–386. 10.1146/annurev-arplant-042817-040440 PubMed DOI

Weckwerth  W, Ghatak  A, Bellaire  A, Chaturvedi  P, Varshney  RK. PANOMICS meets germplasm. Plant Biotechnol J. 2020:18(7):1507–1525. 10.1111/pbi.13372 PubMed DOI PMC

Weng  JK, Ye  M, Li  B, Noel  JP. Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell. 2016:166(4):881–893. 10.1016/j.cell.2016.06.027 PubMed DOI

Wu  Q, Su  N, Huang  X, Cui  J, Shabala  L, Zhou  M, Yu  M, Shabala  S. Hypoxia-induced increase in GABA content is essential for restoration of membrane potential and preventing ROS-induced disturbance to ion homeostasis. Plant Commun. 2021:2(3):100188. 10.1016/j.xplc.2021.100188 PubMed DOI PMC

Yang  W, Feng  H, Zhang  X, Zhang  J, Doonan  JH, Batchelor  WD, Xiong  L, Yan  J. Crop phenomics and high-throughput phenotyping: past decades, current challenges, and future perspectives. Mol Plant. 2020:13(2):187–214. 10.1016/j.molp.2020.01.008 PubMed DOI

Yoshida  T, Fernie  AR. Hormonal regulation of plant primary metabolism under drought. J Exp Bot. 2024:75(6):1714–1725. 10.1093/jxb/erad358 PubMed DOI

Yoshihara  T, Omir  E-SA, Koshino  H, Sakamura  S, Kkuta  Y, Koda  Y. Structure of a tuber-inducing stimulus from potato leaves (Solanum tuberosum L.). Agric Biol Chem. 1989:53(10):2835–2837. 10.1080/00021369.1989.10869712 DOI

Zagoršcak  M, Blejec  A, Ramšak  Ž, Petek  M, Stare  T, Gruden  K. DiNAR: revealing hidden patterns of plant signalling dynamics using Differential Network Analysis in R. Plant Methods. 2018:14:78. PubMed PMC

Zaki  HEM, Radwan  KSA. Response of potato (Solanum tuberosum L.) cultivars to drought stress under in vitro and field conditions. Chem Biol Technol Agric. 2022:9(1):1. 10.1186/s40538-021-00266-z DOI

Zandalinas  SI, Fritschi  FB, Mittler  R. Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends Plant Sci. 2021:26(6):588–599. 10.1016/j.tplants.2021.02.011 PubMed DOI

Zandalinas  SI, Peláez-Vico  MA, Sinha  R, Pascual  LS, Mittler  R. The impact of multifactorial stress combination on plants, crops, and ecosystems: how should we prepare for what comes next?  Plant J. 2023:117(6):1800–1814. 10.1111/tpj.16557 PubMed DOI

Zeng  ZL, Wang  XQ, Zhang  SB, Huang  W. Mesophyll conductance limits photosynthesis in fluctuating light under combined drought and heat stresses. Plant Physiol. 2024:194(3):1498–1511. 10.1093/plphys/kiad605 PubMed DOI

Zhang  H, Sonnewald  U. Differences and commonalities of plant responses to single and combined stresses. Plant J. 2017:90(5):839–855. 10.1111/tpj.13557 PubMed DOI

Zhang  H, Zhu  J, Gong  Z, Zhu  JK. Abiotic stress responses in plants. Nat Rev Genet. 2022a:23(2):104–119. 10.1038/s41576-021-00413-0 PubMed DOI

Zhang  R, Zhang  C, Yu  C, Dong  J, Hu  J. Integration of multi-omics technologies for crop improvement: status and prospects. Front Bioinform. 2022b:2:1027457. 10.3389/fbinf.2022.1027457 PubMed DOI PMC

Zhang  X, Smits  AH, Van Tilburg  GB, Ovaa  H, Huber  W, Vermeulen  M. Proteome-wide identification of ubiquitin interactions using UbIA-MS. Nat Protoc. 2018:13:530–550. 10.1038/nprot.2017.147 PubMed DOI

Zhao  Y, Zhang  W, Abou-Elwafa  SF, Shabala  S, Xu  L. Understanding a mechanistic basis of ABA involvement in plant adaptation to soil flooding: the current standing. Plants (Basel). 2021:10(10):1982. 10.3390/plants10101982 PubMed DOI PMC