Heat stress response mechanisms in pollen development
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Review
PubMed
33818773
PubMed Central
PMC9292940
DOI
10.1111/nph.17380
Knihovny.cz E-resources
- Keywords
- heat stress (HS), heat stress response (HSR), multiomics, pollen development, thermotolerance,
- MeSH
- Stress, Physiological MeSH
- Pollen MeSH
- Heat-Shock Response MeSH
- Plant Breeding * MeSH
- Thermotolerance * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
Being rooted in place, plants are faced with the challenge of responding to unfavourable local conditions. One such condition, heat stress, contributes massively to crop losses globally. Heatwaves are predicted to increase, and it is of vital importance to generate crops that are tolerant to not only heat stress but also to several other abiotic stresses (e.g. drought stress, salinity stress) to ensure that global food security is protected. A better understanding of the molecular mechanisms that underlie the temperature stress response in pollen will be a significant step towards developing effective breeding strategies for high and stable production in crop plants. While most studies have focused on the vegetative phase of plant growth to understand heat stress tolerance, it is the reproductive phase that requires more attention as it is more sensitive to elevated temperatures. Every phase of reproductive development is affected by environmental challenges, including pollen and ovule development, pollen tube growth, male-female cross-talk, fertilization, and embryo development. In this review we summarize how pollen is affected by heat stress and the molecular mechanisms employed during the stress period, as revealed by classical and -omics experiments.
See more in PubMed
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. Sexual Plant Reproduction 18: 91–100.
Ahmed FE, Hall AE, DeMason DA. 1992. Heat injury during floral development in cowpea (Vigna unguiculata, Fabaceae). American Journal of Botany 79: 784–791.
Anderson SN, Johnson CS, Jones DS, Conrad LJ, Gou XP, Russell SD, Sundaresan V. 2013. Transcriptomes of isolated Oryza sativa gametes characterized by deep sequencing: evidence for distinct sex‐dependent chromatin and epigenetic states before fertilization. The Plant Journal 76: 729–741. PubMed
Bao Y, Howell SH. 2017. The unfolded protein response supports plant development and defense as well as responses to abiotic stress. Frontiers in Plant Science 8: 344. PubMed PMC
Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA. 2003. Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiology 133: 713–725. PubMed PMC
Begcy K, Dresselhaus T. 2018. Epigenetic responses to abiotic stresses during reproductive development in cereals. Plant Reproduction 31: 343–355. PubMed PMC
Begcy K, Nosenko T, Zhou LZ, Fragner L, Weckwerth W, Dresselhaus T. 2019. Male sterility in maize after transient heat stress during the tetrad stage of pollen development. Plant Physiology 181: 683–700. PubMed PMC
Berger F, Twell D. 2011. Germline specification and function in plants. Annual Review of Plant Biology 62: 461–484. PubMed
Billey E, Hafidh S, Cruz‐Gallardo I, Litholdo CG, Jean V, Carpentier M‐C, Picart C, Kulichova K, Honys D, Deragon J‐M et al. 2020. LARP6C regulates selective mRNA translation to promote pollen tube guidance in Arabidopsis thaliana . bioRxiv: doi: 10.1101/2020.11.27.401307. PubMed DOI
Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H. 2006. Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiology 140: 1151–1168. PubMed PMC
Bokszczanin KL, Krezdorn N, Fragkostefanakis S, Müller S, Rycak L, Chen Y, Hoffmeier K, Kreutz J, Paupière MJ, Chaturvedi P et al. 2015. Identification of novel small ncRNAs in pollen of tomato. BMC Genomics 16: 714. PubMed PMC
Bokszczanin KL, Fragkostefanakis S; Consortium SPINS‐I . 2013. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Frontiers in Plant Science 4: 315. PubMed PMC
Bokvaj P, Hafidh S, Honys D. 2015. Transcriptome profiling of male gametophyte development in Nicotiana tabacum . Genom Data 3: 106–111. PubMed PMC
Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo JA, Becker JD. 2008. Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiology 148: 1168–1181. PubMed PMC
Boyko A, Filkowski J, Kovalchuk I. 2005. Homologous recombination in plants is temperature and day‐length dependent. Mutation Research–Fundamental and Molecular Mechanisms of Mutagenesis 572: 73–83. PubMed
Calarco J, Borges F, Donoghue M, Van Ex F, Jullien P, Lopes T, Gardner R, Berger F, Feijó JA, Becker JD et al. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151: 194–205. PubMed PMC
Carrizo García C, Nepi M, Pacini E. 2017. It is a matter of timing: asynchrony during pollen development and its consequences on pollen performance in angiosperms – a review. Protoplasma 254: 57–73. PubMed
Chantarachot T, Bailey‐Serres J. 2017. Polysomes, stress granules and processing bodies: a dynamic triumvirate controlling cytoplasmic mRNA fate and function. Plant Physiology 176: 254–269. PubMed PMC
Chaturvedi P, Doerfler H, Jegadeesan S, Ghatak A, Pressman E, Castillejo MA, Wienkoop S, Egelhofer V, Firon N, Weckwerth W. 2015. Heat‐treatment‐responsive proteins in different developmental stages of tomato pollen detected by targeted mass accuracy precursor alignment (tMAPA). Journal of Proteome Research 14: 4463–4471. PubMed
Chaturvedi P, Ghatak A, Weckwerth W. 2016. Pollen proteomics: from stress physiology to developmental priming. Plant Reproduction 29: 119–132. PubMed PMC
Chaturvedi P, Ischebeck T, Egelhofer V, Lichtscheidl I, Weckwerth W. 2013. Cell‐specific analysis of the tomato pollen proteome from pollen mother cell to mature pollen provides evidence for developmental priming. Journal of Proteome Research 12: 4892–4903. PubMed
Chen D, Shao Q, Yin L, Younis A, Zheng B. 2018. Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Frontiers Plant Science 9: 1945. PubMed PMC
Chen Y, Liu P, Hoehenwarter W, Lin J. 2012. Proteomic and phosphoproteomic analysis of Picea wilsonii pollen development under nutrient limitation. Journal of Proteome Research 11: 4180–4190. PubMed
Chen Y, Muller F, Rieu I, Winter P. 2016. Epigenetic events in plant male germ cell heat stress responses. Plant Reproduction 29: 21–29. PubMed
Chen Y, Zou T, McCormick S. 2016. S‐adenosylmethionine synthetase 3 is important for pollen tube growth. Plant Physiology 172: 244–253. PubMed PMC
Conze LL, Berlin S, Le Bail A, Kost B. 2017. Transcriptome profiling of tobacco (Nicotiana tabacum) pollen and pollen tubes. BMC Genomics 18: 581. PubMed PMC
Dai S, Li L, Chen T, Chong K, Xue Y, Wang T. 2006. Proteomic analyses of Oryza sativa mature pollen reveal novel proteins associated with pollen germination and tube growth. Proteomics 6: 2504–2529. PubMed
Dai S, Wang T, Yan X, Chen S. 2007. Proteomics of pollen development and germination. Journal of Proteome Research 6: 4556–4563. PubMed
Dane F, Hunter AG, Cahambliss OL. 1991. Fruit set, pollen fertility, and combining ability of selected tomato genotypes under high‐temperature field conditions. Journal of the American Society for Horticultural Science 116: 906–910.
Davidson RM, Hansey CN, Gowda M, Childs KL, Lin H, Vaillancourt B, Sekhon RS, de Leon N, Kaeppler SM, Jiang N et al. 2011. Utility of RNA sequencing for analysis of maize reproductive transcriptomes. Plant Genome 4: 191–203.
De Storme N, Geelen D. 2013. Cytokinesis in plant male meiosis. Plant Signaling & Behavior 8: e23394. PubMed PMC
De Storme N, Geelen D. 2014. The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant, Cell & Environment 37: 1–18. PubMed PMC
De Storme N, Geelen D. 2020. High temperatures alter cross‐over distribution and induce male meiotic restitution in Arabidopsis thaliana . Communications Biology 3: 187. PubMed PMC
Deng Y, Humbert S, Liu J, Srivastava R, Rothstein S, Howell SH. 2011. Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proceedings of the National Academy of Sciences, USA 108: 7247–7252. PubMed PMC
Deng Y, Srivastava R, Quilichini TD, Dong H, Bao Y, Horner HT, Howell SH. 2016. IRE1, a component of the unfolded protein response signaling pathway, protects pollen development in Arabidopsis from heat stress. The Plant Journal 88: 193–204. PubMed
Devasirvatham V, Gaur PM, Mallikarjuna N, Tokachichu RN, Trethowan RM, Tan DKY. 2012. Effect of high temperature on the reproductive development of chickpea genotypes under controlled environments. Functional Plant Biology 39: 1009–1018. PubMed
Ding XL, Wang X, Li Q, Yu LF, Song QJ, Gai JY, Yang SP. 2019. Metabolomics studies on cytoplasmic male sterility during flower bud development in soybean. International Journal of Molecular Sciences 20: 2869. PubMed PMC
Djanaguiraman M, Vara Prasad PV, Murugan M, Perumal R, Reddy UK. 2014. Physiological differences among sorghum (Sorghum bicolor L. Moench) genotypes under high temperature stress. Environmental and Experimental Botany 100: 43–54.
Driedonks N, Wolters‐Arts M, Huber H, de Boer G‐J, Vriezen W, Mariani C, Rieu I. 2018. Exploring the natural variation for reproductive thermotolerance in wild tomato species. Euphytica 214: 67.
Fernando DD. 2005. Characterization of pollen tube development in Pinus strobus (Eastern white pine) through proteomic analysis of differentially expressed proteins. Proteomics 5: 4917–4926. PubMed
Fíla J, Matros A, Radau S, Zahedi RP, Čapková V, Mock H‐P, Honys D. 2012. Revealing phosphoproteins playing role in tobacco pollen activated in vitro . Proteomics 12: 3229–3250. PubMed
Fíla J, Radau S, Matros A, Hartmann A, Scholz U, Feciková J, Mock HP, Čapková V, Zahedi RP, Honys D. 2016. Phosphoproteomics profiling of tobacco mature pollen and pollen activated in vitro . Molecular & Cellular Proteomics 15: 1338–1350. PubMed PMC
Fíla J, Záveská Drábková L, Gibalová A, Honys D. 2017. When simple meets complex: pollen and the ‐omics. In: Obermeyer G, Feijó J, eds. Pollen tip growth . Cham, Switzerland: Springer, 247–292.
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 PMC
Foolad MR, Sharma A. 2005. Molecular markers as selection tools in tomato breeding. Acta Horticulturae 695: 225–240.
Fotovat R, Alikhani M, Valizadeh M, Mirzaei M, Salekdeh GH. 2017. A proteomics approach to discover drought tolerance proteins in wheat pollen grain at meiosis stage. Protein and Peptide Letters 24: 26–36. PubMed
Fragkostefanakis S, Mesihovic A, Hu Y, Schleiff E. 2016a. Unfolded protein response in pollen development and heat stress tolerance. Plant Reproduction 29: 81–91. PubMed
Fragkostefanakis S, Mesihovic A, Simm S, Paupière MJ, Hu Y, Paul P, Mishra SK, Tschiersch B, Theres K, Bovy A et al. 2016b. HsfA2 controls the activity of developmentally and stress‐regulated heat stress protection mechanisms in tomato male reproductive tissues. Plant Physiology 170: 2461–2477. PubMed PMC
Fragkostefanakis S, Roth S, Schleiff E, Scharf KD. 2015. Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant, Cell & Environment 38: 1881–1895. PubMed
Francis KE, Lam SY, Harrison BD, Bey AL, Berchowitz LE, Copenhaver GP. 2007. Pollen tetrad‐based visual assay for meiotic recombination in Arabidopsis. Proceedings of the National Academy of Sciences, USA 104: 3913–3918. PubMed PMC
Gao Y‐B, Wang C‐L, Wu J‐Y, Zhou H‐S, Jiang X‐T, Wu J, Zhang S‐L. 2014. Low temperature inhibits pollen tube growth by disruption of both tip‐localized reactive oxygen species and endocytosis in Pyrus bretschneideri Rehd. Plant Physiology and Biochemistry 74: 255–262. PubMed
Ghatak A, Chaturvedi P, Weckwerth W. 2018. Metabolomics in plant stress physiology. Plant Genetics and Molecular Biology 164: 187–236. PubMed
Gibson SI. 2004. Sugar and phytohormone response pathways: navigating a signalling network. Journal of Experimental Botany 55: 253–264. PubMed
Giorno F, Wolters‐Arts M, Grillo S, Scharf K‐D, Vriezen WH, Mariani C. 2010. Developmental and heat stress‐regulated expression of HsfA2 and small heat shock proteins in tomato anthers. Journal of Experimental Botany 61: 453–462. PubMed PMC
Giorno F, Wolters‐Arts M, Mariani C, Rieu I. 2013. Ensuring reproduction at high temperatures: the heat stress response during anther and pollen development. Plants 2: 489–506. PubMed PMC
Gomez A, Lopez JA, Pintos B, Camafeita E, Bueno MA. 2009. Proteomic analysis from haploid and diploid embryos of Quercus suber L. identifies qualitative and quantitative differential expression patterns. Proteomics 9: 4355–4367. PubMed
Grandillo S, Chetelat R, Knapp S, Spooner D, Peralta I, Cammareri M, Perez O, Termolino P, Tripodi P, Chiusano ML. 2007. Solanum sect. Lycopersicon. In: Kole C, ed. Wild crop relatives: genomic and breeding resources. Heidelberg, Germany; Dordrecht, the Netherlands; London, UK; New York, USA: Springer, 129–215.
Grilli GVG, Braz LT, Lemos EGM. 2007. QTL identification for tolerance to fruit set in tomato by fAFLP markers. Crop Breeding and Applied Biotechnology 7: 234–241.
Grobei MA, Qeli E, Brunner E, Rehrauer H, Zhang RX, Roschitzki B, Basler K, Ahrens CH, Grossniklaus U. 2009. Deterministic protein inference for shotgun proteomics data provides new insights into Arabidopsis pollen development and function. Genome Research 19: 1786–1800. PubMed PMC
Guan Q, Lu X, Zeng H, Zhang Y, Zhu J. 2013. Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. The Plant Journal 74: 840–851. PubMed
Gupta SK, Rai KN, Singh P, Ameta VL, Gupta SK, Jayalekha AK, Mahala RS, Pareek S, Swami ML, Verma YS. 2015. Seed set variability under high temperatures during flowering period in pearl millet (Pennisetum glaucum L. (R.) Br.). Field Crops Research 171: 41–53.
Hafidh S, Breznenova K, Honys D. 2012a. De novo post‐pollen mitosis II tobacco pollen tube transcriptome. Plant Signaling & Behavior 7: 918–921. PubMed PMC
Hafidh S, Breznenova K, Ruzicka P, Fecikova J, Capkova V, Honys D. 2012b. Comprehensive analysis of tobacco pollen transcriptome unveils common pathways in polar cell expansion and underlying heterochronic shift during spermatogenesis. BMC Plant Biology 12: 24. PubMed PMC
Hafidh S, Fila J, Honys D. 2016. Male gametophyte development and function in angiosperms: a general concept. Plant Reproduction 29: 31–51. PubMed
Hafidh S, Potěšil D, Müller K, Fíla J, Michailidis C, Herrmannová A, Feciková J, Ischebeck T, Valášek LS, Zdráhal Z et al. 2018. Dynamics of the pollen sequestrome defined by subcellular coupled omics. Plant Physiology 178: 258–282. PubMed PMC
Hamid R, Marashi H, Tomar RS, Shafaroudi SM, Sabara PH. 2019. Transcriptome analysis identified aberrant gene expression in pollen developmental pathways leading to CGMS in cotton (Gossypium hirsutum L.). PLoS ONE 14: e0218381. PubMed PMC
Han B, Chen SX, Dai SJ, Yang N, Wang T. 2010. Isobaric tags for relative and absolute quantification‐based comparative proteomics reveals the features of plasma membrane‐associated proteomes of pollen grains and pollen tubes from Lilium davidii . Journal of Integrative Plant Biology 52: 1043–1058. PubMed
Harsant J, Pavlovic L, Chiu G, Sultmanis S, Sage TL. 2013. High temperature stress and its effect on pollen development and morphological components of harvest index in the C3 model grass Brachypodium distachyon . Journal of Experimental Botany 64: 2971–2983. PubMed PMC
Hedhly A. 2011. Sensitivity of flowering plant gametophytes to temperature fluctuations. Environmental & Experimental Botany 74: 9–16.
Holmes‐Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S. 2005. Proteome mapping of mature pollen of Arabidopsis thaliana . Proteomics 5: 4864–4884. PubMed
Hong SW, Vierling E. 2000. Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proceedings of the National Academy of Sciences, USA 97: 4392–4397. PubMed PMC
Honys D, Twell D. 2003. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiology 132: 640–652. PubMed PMC
Honys D, Twell D. 2004. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biology 5: R85. PubMed PMC
Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D. 2011. Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23: 515–533. PubMed PMC
Imin N, Kerim T, Rolfe BG, Weinman JJ. 2004. Effect of early cold stress on the maturation of rice anthers. Proteomics 4: 1873–1882. PubMed
Imin N, Kerim T, Weinman JJ, Rolfe BG. 2006. Low temperature treatment at the young microspore stage induces protein changes in rice anthers. Molecular & Cellular Proteomics 5: 274–292. PubMed
Ischebeck T, Valledor L, Lyon D, Gingl S, Nagler M, Meijon M, Egelhofer V, Weckwerth W. 2014. Comprehensive cell‐specific protein analysis in early and late pollen development from diploid microsporocytes to pollen tube growth. Molecular & Cellular Proteomics 13: 295–310. PubMed PMC
Ishiguro S, Kawai‐Oda A, Ueda J, Nishida I, Okada K. 2001. The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13: 2191–2209. PubMed PMC
Ismail AM, Hall AE. 1999. Reproductive‐stage heat tolerance, leaf membrane thermostability and plant morphology in cowpea. Crop Science 39: 1762–1768.
Iwata Y, Koizumi N. 2005. An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proceedings of the National Academy of Sciences, USA 102: 5280–5285. PubMed PMC
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.). Journal of Experimental Botany 61: 143–156. PubMed PMC
Jegadeesan S, Chaturvedi P, Ghatak A, Pressman E, Meir S, Faigenboim A, Rutley N, Beery A, Harel A, Weckwerth W et al. 2018. Proteomics of heat‐stress and ethylene‐mediated thermotolerance mechanisms in tomato pollen grains. Frontiers in Plant Science 9: 1558. PubMed PMC
Ji X, Dong B, Shiran B, Talbot MJ, Edlington JE, Hughes T, White RG, Gubler F, Dolferus R. 2011. Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiology 156: 647–662. PubMed PMC
Jiang J, Liu X, Liu C, Liu G, Li S, Wang L. 2017. Integrating omics and alternative splicing reveals insights into grape response to high temperature. Plant Physiology 173: 1502–1518. PubMed PMC
Jiang Y, Lahlali R, Karunakaran C, Warkentin TD, Davis AR, Bueckert RA. 2019. Pollen, ovules, and pollination in pea: success, failure, and resilience in heat. Plant, Cell & Environment 42: 354–372. PubMed
Julca I, Ferrari C, Flores‐Tornero M, Proost S, Lindner A‐C, Hackenberg D, Steinbachová L, Michaelidis C, Pereira SG, Misra CS et al. 2020. Comparative transcriptomic analysis reveals conserved transcriptional programs underpinning organogenesis and reproduction in land plants. bioRxiv. doi: 10.1101/2020.10.29.361501. PubMed DOI
Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL. 2004. Exploring the temperature‐stress metabolome of Arabidopsis. Plant Physiology 136: 4159–4168. PubMed PMC
Karapanos IC, Akoumianakis KA, Olympios CM, Passam HC. 2009. The effect of substrate, ADP and uncoupler on the respiration of tomato pollen during incubation in vitro at moderately high temperature. Sexual Plant Reproduction 22: 133–140. PubMed
Keller M, Hu Y, Mesihovic A, Fragkostefanakis S, Schleiff E, Simm S. 2017. Alternative splicing in tomato pollen in response to heat stress. DNA Research 24: 205–217. PubMed PMC
Keller M, Simm S. 2018. The coupling of transcriptome and proteome adaptation during development and heat stress response of tomato pollen. BMC Genomics 19: 447. PubMed PMC
Kerim T, Imin N, Weinman JJ, Rolfe BG. 2003. Proteome analysis of male gametophyte development in rice anthers. Proteomics 3: 738–751. PubMed
Khatun S, Flowers TJ. 1995. The estimation of pollen viability in rice. Journal of Experimental Botany 46: 151–154.
Kim M, Kim H, Lee W, Lee Y, Kwon SW, Lee J. 2015. Quantitative shotgun proteomics analysis of rice anther proteins after exposure to high temperature. International Journal of Genomics 2015: 1–9. PubMed PMC
Kosmacz M, Gorka M, Schmidt S, Luzarowski M, Moreno JC, Szlachetko J, Leniak E, Sokolowska EM, Sofroni K, Schnittger A et al. 2019. Protein and metabolite composition of Arabidopsis stress granules. New Phytologist 222: 1420–1433. PubMed
Kotak S, Larkindale J, Lee U, von Koskull‐Doring P, Vierling E, Scharf KD. 2007. Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10: 310–316. PubMed
Kranner I, Minibayeva FV, Beckett RP, Seal CE. 2010. What is stress? Concepts, definitions and applications in seed science. New Phytologist 188: 655–673. PubMed
Kumar RR, Goswami S, Gadpayle KA, Singh K, Sharma SK, Singh GP, Pathak H, Rai RD. 2014. Ascorbic acid at pre‐anthesis modulate the thermotolerance level of wheat (Triticum aestivum) pollen under heat stress. Journal of Plant Biochemistry and Biotechnology 23: 293–306.
Kumar S, Thakur P, Kaushal N, Malik JA, Gaur P, Nayyar H. 2013. Effect of varying high temperatures during reproductive growth on reproductive function, oxidative stress and seed yield in chickpea genotypes differing in heat sensitivity. Archives of Agronomy and Soil Science 59: 823–843.
Kurusu T, Kuchitsu K. 2017. Autophagy, programmed cell death and reactive oxygen species in sexual reproduction in plants. Journal of Plant Research 130: 491–499. PubMed
Lang‐Mladek C, Popova O, Kiok K, Berlinger M, Rakic B, Aufsatz W, Jonak C, Hauser MT, Luschnig C. 2010. Transgenerational inheritance and resetting of stress‐induced loss of epigenetic gene silencing in Arabidopsis. Molecular Plant 3: 594–602. PubMed PMC
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 Physiology 138: 882–897. PubMed PMC
Larkindale J, Vierling E. 2008. Core genome responses involved in acclimation to high temperature. Plant Physiology 146: 748–761. PubMed PMC
Lee SS, Jung WY, Park HJ, Lee A, Kwon SY, Kim HS, Cho HS. 2018. Genome‐wide analysis of alternative splicing in an inbred cabbage (Brassica oleracea L.) line 'HO' in response to heat stress. Current Genomics 19: 12–20. PubMed PMC
Lee JY, Lee DH. 2003. Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiology 132: 517–529. PubMed PMC
Lee S‐LJ, Warmke HE. 1979. Organelle size and number in fertile and T‐cytoplasmic male‐sterile corn. American Journal of Botany 66: 141–148.
Lewandowska D, Zhang R, Colas I, Uzrek N, Waugh R. 2019. Application of a sensitive and reproducible label‐free proteomic approach to explore the proteome of individual meiotic‐phase barley anthers. Frontiers in Plant Science 10: 393. PubMed PMC
Li SM, Su XQ, Abdullah M, Sun YM, Li GH, Cheng X, Lin Y, Cai YP, Jin Q. 2018. Effects of different pollens on primary metabolism and lignin biosynthesis in pear. International Journal of Molecular Sciences 19: 2273. PubMed PMC
Li Y‐F, Wang Y, Tang Y, Gobal Kakani V, Mahalingam R. 2013. Transcriptome analysis of heat stress response in switchgrass (Panicum virgatum L.). BMC Plant Biology 13: 153. PubMed PMC
Li Y‐F, Zheng Y, Vemireddy LR, Panda SK, Jose S, Ranjan A, Panda P, Govindan G, Cui J, Wei K et al. 2018. Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt‐tolerant Pokkali under salt stress. BMC Genomics 19: 935. PubMed PMC
Li ZJ, Zhang PP, Lv JY, Cheng YF, Cui JM, Zhao HX, Hu SW. 2016. Global dynamic transcriptome programming of rapeseed (Brassica napus L.) anther at different development stages. PLoS ONE 11: e0154039. PubMed PMC
Lin SY, Chen PW, Chuang MH, Juntawong P, Bailey‐Serres J, Jauh GY. 2014. Profiling of translatomes of in vivo‐grown pollen tubes reveals genes with roles in micropylar guidance during pollination in Arabidopsis. Plant Cell 26: 602–618. PubMed PMC
Liu HC, Liao HT, Charng YY. 2011. The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant, Cell & Environment 34: 738–751. PubMed
Liu J, Pang C, Wei H, Song M, Meng Y, Ma J, Fan S, Yu S. 2015. iTRAQ‐facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild‐type cotton (Gossypium hirsutum L.). Journal of Proteomics 126: 68–81. PubMed
Liu JX, Bennett J. 2011. Reversible and irreversible drought‐induced changes in the anther proteome of rice (Oryza sativa L.) genotypes IR64 and Moroberekan. Molecular Plant 4: 59–69. PubMed
Liu JX, Howell SH. 2010. bZIP28 and NF‐Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell 22: 782–796. PubMed PMC
Liu JX, Srivastava R, Che P, Howell SH. 2007. An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane‐associated transcription factor, bZIP28. Plant Cell 19: 4111–4119. PubMed PMC
Lobell DB, Bänziger M, Magorokosho C, Vivek B. 2011. Nonlinear heat effects on African maize as evidenced by historical yield trials. Nature Climate Change 1: 42–45.
Loraine AE, McCormick S, Estrada A, Patel K, Qin P. 2013. RNA‐Seq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiology 162: 1092–1109. PubMed PMC
Luria G, Rutley N, Lazar I, Harper JF, Miller G. 2019. Direct analysis of pollen fitness by flow cytometry: implications for pollen response to stress. The Plant Journal 98: 942–952. PubMed
Matsuura H, Ishibashi Y, Shinmyo A, Kanaya S, Kato K. 2010. Genome‐wide analyses of early translational responses to elevated temperature and high salinity in Arabidopsis thaliana . Plant and Cell Physiology 51: 448–462. PubMed
Mazzeo MF, Cacace G, Iovieno P, Massarelli I, Grillo S, Siciliano RA. 2018. Response mechanisms induced by exposure to high temperature in anthers from thermo‐tolerant and thermo‐sensitive tomato plants: a proteomic perspective. PLoS ONE 13: e0201027. PubMed PMC
McCue AD, Panda K, Nuthikattu S, Choudury SG, Thomas EN, Slotkin RK. 2015. ARGONAUTE 6 bridges transposable element mRNA‐derived siRNAs to the establishment of DNA methylation. EMBO Journal 34: 20–35. PubMed PMC
Mesihovic A, Iannacone R, Firon N, Fragkostefanakis S. 2016. Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reproduction 29: 93–105. PubMed
Migicovsky Z, Yao Y, Kovalchuk I. 2014. Transgenerational phenotypic and epigenetic changes in response to heat stress in Arabidopsis thaliana . Plant Signal Behaviour 9: e27971. PubMed PMC
Mishra RC, Grover A. 2015. ClpB/Hsp100 proteins and heat stress tolerance in plants. Critical Reviews in Biotechnology 36: 862–874. PubMed
Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD. 2002. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes & Development 16: 1555–1567. PubMed PMC
Mitchell JC, Petolino JF. 1988. Heat stress effects on isolated reproductive organs of maize. Journal of Plant Physiology 133: 625–628.
Mittler R. 2017. ROS are good. Trends Plant Science 22: 11–19. PubMed
Mittler R, Finka A, Goloubinoff P. 2012. How do plants feel the heat? Trends in Biochemical Sciences 37: 118–125. PubMed
Muller F, Rieu I. 2016. Acclimation to high temperature during pollen development. Plant Reproduction 29: 107–118. PubMed PMC
Nägele T, Fragner L, Chaturvedi P, Ghatak A, Weckwerth W. 2017. Pollen metabolome dynamics: biochemistry, regulation and analysis. In: Obermeyer G, Feijó J, eds. Pollen tip growth. Cham, Switzerland: Springer, 319–336.
Náprstková A, Malínská K, Záveská Drábková L, Billey E, Náprstková D, Sýkorová E, Bousquet‐Antonelli C, Honys D. 2021. Characterization of ALBA family expression and localization in Arabidopsis thaliana generative organs. International Journal of Molecular Sciences 22: 1652. PubMed PMC
Noir S, Brautigam A, Colby T, Schmidt J, Panstruga R. 2005. A reference map of the Arabidopsis thaliana mature pollen proteome. Biochemical and Biophysical Research Communications 337: 1257–1266. PubMed
Obermeyer G, Fragner L, Lang V, Weckwerth W. 2013. Dynamic adaption of metabolic pathways during germination and growth of lily pollen tubes after inhibition of the electron transport chain. Plant Physiology 162: 1822–1833. PubMed PMC
Oda S, Kaneko F, Yano K, Fujioka T, Masuko H, Park J‐I, Kikuchi S, Hamada K, Endo M, Nagano K et al. 2010. Morphological and gene expression analysis under cool temperature conditions in rice anther development. Genes & Genetic Systems 85: 107–120. PubMed
Ohama N, Sato H, Shinozaki K, Yamaguchi‐Shinozaki K. 2017. Transcriptional regulatory network of plant heat stress response. Trends in Plant Science 22: 53–65. PubMed
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. Molecular Genetics and Genomics 278: 31–42. PubMed
Parrotta L, Faleri C, Cresti M, Cai G. 2016. Heat stress affects the cytoskeleton and the delivery of sucrose synthase in tobacco pollen tubes. Planta 243: 43–63. PubMed
Paul P, Chaturvedi P, Selymesi M, Ghatak A, Mesihovic A, Scharf KD, Weckwerth W, Simm S, Schleiff E. 2016. The membrane proteome of male gametophyte in Solanum lycopersicum . Journal of Proteomics 131: 48–60. PubMed
Paupière MJ, van Haperen P, Rieu I, Visser RGF, Tikunov YM, Bovy AG. 2017b. Screening for pollen tolerance to high temperatures in tomato. Euphytica 213: 130.
Paupiere MJ, van Heusden AW, Bovy AG. 2014. The metabolic basis of pollen thermo‐tolerance: perspectives for breeding. Metabolites 4: 889–920. PubMed PMC
Paupière MJ, Muller F, Li HJ, Rieu I, Tikunov YM, Visser RGF, Bovy AG. 2017a. Untargeted metabolomic analysis of tomato pollen development and heat stress response. Plant Reproduction 30: 81–94. PubMed PMC
Pazhamala LT, Chaturvedi P, Bajaj P, Srikanth S, Ghatak A, Chitikineni A, Bellaire A, Hingane A, Kumar CVS, Saxena Kb et al. 2020. Multiomics approach unravels fertility transition in a pigeonpea line for a two‐line hybrid system. Plant Genome 13: e20028. PubMed
Pecinka A, Mittelsten SO. 2012. Stress‐induced chromatin changes: a critical view on their heritability. Plant and Cell Physiology 53: 801–808. PubMed PMC
Pecrix Y, Rallo G, Folzer H, Cigna M, Gudin S, Le Bris M. 2011. Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. Journal of Experimental Botany 62: 3587–3597. PubMed
Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG. 2004. Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences, USA 101: 9971–9975. PubMed PMC
Pertl H, Pockl M, Blaschke C, Obermeyer G. 2010. Osmoregulation in lilium pollen grains occurs via modulation of the plasma membrane H+ ATPase activity by 14‐3‐3 proteins. Plant Physiology 154: 1921–1928. PubMed PMC
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. PubMed PMC
Poidevin L, Forment J, Unal D, Ferrando A. 2020. Transcriptome and translatome changes in germinated pollen under heat stress uncover roles of transporter genes involved in pollen tube growth. Plant, Cell & Environment. doi: 10.1111/pce.13972. PubMed DOI
Pressman E, Harel D, Zamski E, Shaked R, Althan L, Rosenfeld K, Firon N. 2006. The effect of high temperatures on the expression and activity of sucrose‐cleaving enzymes during tomato (Lycopersicon esculentum) anther development. Journal of Horticultural Science and Biotechnology 81: 341–348.
Pressman E, Peet MM, Pharr DM. 2002. The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Annals of Botany 90: 631–636. PubMed PMC
Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R. 2009. Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genetics 5: e1000621. PubMed PMC
Qu AL, Ding YF, Jiang Q, Zhu C. 2013. Molecular mechanisms of the plant heat stress response. Biochemical and Biophysical Research Communications 432: 203–207. PubMed
Rahmati Ishka M, Brown E, Weigand C, Tillett RL, Schlauch KA, Miller G, Harper JF. 2018. A comparison of heat‐stress transcriptome changes between wild‐type Arabidopsis pollen and a heat‐sensitive mutant harboring a knockout of cyclic nucleotide‐gated cation channel 16 (cngc16). BMC Genomics 19: 549. PubMed PMC
Raja MM, Vijayalakshmi G, Naik ML, Basha PO, Sergeant K, Hausman JF, Khan PSSV. 2019. Pollen development and function under heat stress: from effects to responses. Acta Physiologiae Plantarum 41: 47.
Reňák D, Gibalová A, Šolcová K, Honys D. 2014. A new link between stress response and nucleolar function during pollen development in Arabidopsis mediated by AtREN1 protein. Plant, Cell & Environment 37: 670–683. PubMed
Rice‐Evans CA, Miller NJ, Paganga G. 1996. Structure‐antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biology and Medicine 20: 933–956. PubMed
Rieu I, Twell D, Firon N. 2017. Pollen development at high temperature: from acclimation to collapse. Plant Physiology 173: 1967–1976. PubMed PMC
Rizhsky L, Liang H, Mittler R. 2002. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology 130: 1143–1151. PubMed PMC
Rotsch AH, Kopka J, Feussner I, Ischebeck T. 2017. Central metabolite and sterol profiling divides tobacco male gametophyte development and pollen tube growth into eight metabolic phases. The Plant Journal 92: 129–146. PubMed
Rutley N, Twell D. 2015. A decade of pollen transcriptomics. Plant Reproduction 28: 73–89. PubMed PMC
Saini HS, Sedgley M, Aspinall D. 1984. Developmental anatomy in wheat of male‐sterility induced by heat‐stress, water deficit or abscisic‐acid. Australian Journal of Plant Physiology 11: 243–253.
Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, Higashitani N, Miyazawa Y, Takahashi H, Watanabe M, Higashitani A. 2010. Auxins reverse plant male sterility caused by high temperatures. Proceedings of the National Academy of Sciences, USA 107: 8569–8574. PubMed PMC
Sarhadi E, Bazargani MM, Sajise AG, Abdolahi S, Vispo NA, Arceta M, Nejad GM, Singh RK, Salekdeh GH. 2012. Proteomic analysis of rice anthers under salt stress. Plant Physiology and Biochemistry 58: 280–287. PubMed
Scarpin MR, Sigaut L, Temprana SG, Boccaccio GL, Pietrasanta LI, Muschietti JP. 2017. Two Arabidopsis late pollen transcripts are detected in cytoplasmic granules. Plant Direct 1: 4. PubMed PMC
Scharf KD, Berberich T, Ebersberger I, Nover L. 2012. The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochimica et Biophysica Acta 1819: 104–119. PubMed
Schmidt A, Schmid MW, Grossniklaus U. 2012. Analysis of plant germline development by high‐throughput RNA profiling: technical advances and new insights. The Plant Journal 70: 18–29. PubMed
Selinski J, Scheibe R. 2014. Pollen tube growth: where does the energy come from? Plant Signaling & Behavior 9: e977200. PubMed PMC
Sharma P, Jha AB, Dubey RS, Pessarakli M. 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012: 1–26.
Sheoran IS, Pedersen EJ, Ross ARS, Sawhney VK. 2009. Dynamics of protein expression during pollen germination in canola (Brassica napus). Planta 230: 779–793. PubMed
Sheoran IS, Ross ARS, Olson DJH, Sawhney VK. 2007. Proteomic analysis of tomato (Lycopersicon esculentum) pollen. Journal of Experimental Botany 58: 3525–3535. PubMed
Sheth BP, Thaker VS. 2014. Plant systems biology: insights, advances and challenges. Planta 240: 33–54. PubMed
Shishova M, Puzanskiy R, Gavrilova O, Kurbanniazov S, Demchenko K, Yemelyanov V, Pendinen G, Shavarda A, Gavrilenko T. 2019. Metabolic alterations in male‐sterile potato as compared to male‐fertile. Metabolites 9: 24. PubMed PMC
Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461–472. PubMed PMC
Solis MT, Rodriguez‐Serrano M, Meijon M, Canal MJ, Cifuentes A, Risueno MC, Testillano PS. 2012. DNA methylation dynamics and MET1a‐like gene expression changes during stress‐induced pollen reprogramming to embryogenesis. Journal of Experimental Botany 63: 6431–6444. PubMed PMC
Song L, Liu Z, Tong J, Xiao L, Ma H, Zhang H. 2015. Comparative proteomics analysis reveals the mechanism of fertility alternation of thermosensitive genic male sterile rice lines under low temperature inducement. Proteomics 15: 1884–1905. PubMed
Stone PJ, Nicolas ME. 1995. A survey of the effects of high‐temperature during grain filling on yield and quality of 75 wheat cultivars. Australian Journal of Agricultural Research 46: 475–492.
Suzuki K, Tsukaguchi T, Takeda H, Egawa Y. 2001. Decrease of pollen stainability of green bean at high temperatures and relationship to heat tolerance. Journal of the American Society for Horticultural Science 126: 571–574.
Tang HL, Song YL, Guo JL, Wang JW, Zhang LL, Niu N, Ma SC, Zhang GS, Zhao HY. 2018. Physiological and metabolome changes during anther development in wheat (Triticum aestivum L.). Plant Physiology and Biochemistry 132: 18–32. PubMed
Tashiro T, Wardlaw IF. 1989. A comparison of the effect of high temperature on grain development in wheat and rice. Annals of Botany 64: 59–65.
Urquidi Camacho RA, Lokdarshi A, von Arnim AG. 2020. Translational gene regulation in plants: a green new deal. WIREs RNA 11: e1597. PubMed PMC
Uvackova L, Takac T, Boehm N, Obert B, Samaj J. 2012. Proteomic and biochemical analysis of maize anthers after cold pretreatment and induction of androgenesis reveals an important role of anti‐oxidative enzymes. Journal of Proteomics 75: 1886–1894. PubMed
Valero Galvan J, Valledor L, Navarro Cerrillo RM, Gil Pelegrin E, Jorrin‐Novo JV. 2011. Studies of variability in Holm oak (Quercus ilex subsp. ballota [Desf.] Samp.) through acorn protein profile analysis. Journal of Proteomics 74: 1244–1255. PubMed
Vierling E. 1991. The roles of heat shock proteins in plants. Annual Review of Plant Biology 42: 579–620.
Wang J, Li D, Shang F, Kang X. 2017. High temperature‐induced production of unreduced pollen and its cytological effects in Populus . Scientific Reports 7: 5281. PubMed PMC
Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH. 2008. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiology 148: 1201–1211. PubMed PMC
Weber C, Nover L, Fauth M. 2008. Plant stress granules and mRNA processing bodies are distinct from heat stress granules. The Plant Journal 56: 517–530. PubMed
Weckwerth W, Ghatak A, Bellaire A, Chaturvedi P, Varshney RK. 2020. PANOMICS meets germplasm. Plant Biotechnology Journal 18: 1507–1525. PubMed PMC
Whittle CA, Malik MR, Li R, Krochko JE. 2010. Comparative transcript analyses of the ovule, microspore, and mature pollen in Brassica napus . Plant Molecular Biology 72: 279–299. PubMed
Wiese AJ, Steinbachová L, Timofejeva L, Čermák V, Klodová B, Ganji RS, Limones‐Mendez M, Bokvaj P, Hafidh S, Potěšil D et al. 2021. Arabidopsis bZIP18 and bZIP52 accumulate in nuclei following heat stress where they regulate the expression of a similar set of genes. International Journal of Molecular Sciences 22: 530. PubMed PMC
Willing RP, Mascarenhas JP. 1984. Analysis of the complexity and diversity of messenger‐RNAS from pollen and shoots of tradescantia. Plant Physiology 75: 865–868. PubMed PMC
Xu J, Zhang B, Jiang C, Ming F. 2011. RceIF5A, encoding an eukaryotic translation initiation factor 5A in Rosa chinensis, can enhance thermotolerance, oxidative and osmotic stress resistance of Arabidopsis thaliana . Plant Molecular Biology 75: 167–178. PubMed
Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, Maruyama K, Kim J‐M, Seki M, Todaka D et al. 2011. Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock‐responsive gene expression. Molecular Genetics and Genomics 286: 321–332. PubMed
Yu SX, Feng QN, Xie HT, Li S, Zhang Y. 2017. Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato. BMC Plant Biology 17: 76. PubMed PMC
Zhang C, Li G, Chen T, Feng B, Fu W, Yan J, Islam MR, Jin Q, Tao L, Fu G. 2018. Heat stress induces spikelet sterility in rice at anthesis through inhibition of pollen tube elongation interfering with auxin homeostasis in pollinated pistils. Rice 11: 14. PubMed PMC
Zhang L, Liu X, Gaikwad K, Kou X, Wang F, Tian X, Xin M, Ni Z, Sun Q, Peng H et al. 2017. Mutations in eIF5B confer thermosensitive and pleiotropic phenotypes via translation defects in Arabidopsis thaliana . Plant Cell 29: 1952–1969. PubMed PMC
Zhang SS, Yang H, Ding L, Song ZT, Ma H, Chang F, 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: 1007–1023. PubMed PMC
Zhang XL, Zhang J, Guo YH, Sun P, Jia HX, Fan W, Lu MZ, Hu JJ. 2016. Comparative proteomic analysis of mature pollen in triploid and diploid Populus deltoides . International Journal of Molecular Sciences 17: 1475. PubMed PMC
Zhang Z, Hu M, Feng X, Gong A, Cheng L, Yuan H. 2017. Proteomes and phosphoproteomes of anther and pollen: availability and progress. Proteomics 17: 1600458. PubMed
Zhao Q, Zhou L, Liu J, Cao Z, Du X, Huang F, Pan G, Cheng F. 2018. Involvement of CAT in the detoxification of HT‐induced ROS burst in rice anther and its relation to pollen fertility. Plant Cell Reports 37: 741–757. PubMed
Zhou B, Liu Y, Chen Z, Liu D, Wang Y, Zheng J, Liao X, Zhou AR. 2019. Comparative transcriptome analysis reveals the cause for accumulation of reactive oxygen species during pollen abortion in cytoplasmic male‐sterile Kenaf line 722HA. International Journal of Molecular Sciences 20: 5515. PubMed PMC
Zhu JK. 2016. Abiotic stress signaling and responses in plants. Cell 167: 313–324. PubMed PMC
Zinn KE, Tunc‐Ozdemir M, Harper JF. 2010. Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany 61: 1959–1968. PubMed PMC
Ziska LH, Manalo PA, Ordonez RA. 1996. Intraspecific variation in the response of rice (Oryza sativa L.) to increased CO2 and temperature: growth and yield response of 17 cultivars. Journal of Experimental Botany 47: 1353–1359.
Priming thermotolerance: unlocking heat resilience for climate-smart crops
"Resilience in crop reproduction for food security: introducing RECROP COST action"
Heat stress impairs centromere structure and segregation of meiotic chromosomes in Arabidopsis
Editorial: Advances in Pollen Research: Biology, Biotechnology, and Plant Breeding Applications