Heat Stress During Gametogenesis Irreversibly Damages Female Reproductive Organ in Rice
Tóm tắt
Heat stress during gametogenesis leads to spikelet sterility. To ascertain the role of female reproductive organ (pistil), two rice genotypes N22 and IR64 with contrasting heat stress responses were exposed to control (30 °C) and heat stress (38 °C and 40 °C) during megasporogenesis. Anatomical observations of ovule revealed greater disappearance of megaspore mother cell and nuclei at early stages, and during later stages mature embryo sac without female germ unit, improper positioning of nuclei, and shrunken embryo sac was observed in the sensitive IR64. Under heat stress, a decrease in sugar and starch, increase in H2O2 and malondialdehyde with lower antioxidant enzyme activities were recorded in pistils of both N22 and IR64. Lower accumulation of TCA cycle metabolites and amino acids were noticed in IR64 pistils under heat stress at gametogenesis, whereas N22 exhibited favorable metabolite profiles. At heading, however, N22 pistils had higher carbohydrate accumulation and better ROS homeostasis, suggesting higher recovery after heat stress exposure. In summary, the results indicate that heat stress during megasporogenesis leads to irreversible anatomical and physiological changes in pistil and alters metabolic signatures leading to increased spikelet sterility in rice. Mechanisms identified for enhanced heat tolerance in pistil can help in developing rice varieties that are better adapted to future hotter climate.
Tài liệu tham khảo
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Arshad MS, Farooq M, Asch F, Jagadish SVK, Prasad PVV, Siddique KH (2017) Thermal stress impacts reproductive development and grain yield in rice. Plant Physiol Biochem 115:57–72. https://doi.org/10.1016/j.plaphy.2017.03.011
Basha G, Kishore P, Ratnam MV, Jayaraman A, Kouchak AA, Ouarda TB, Velicogna I (2017) Historical and projected surface temperature over India during the 20th and 21st century. Sci Rep 7(1):1–10. https://doi.org/10.1038/s41598-017-02130-3
Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 59(3):411–416. https://doi.org/10.1104/pp.59.3.411
Chiluwal A, Bheemanahalli R, Kanaganahalli V, Boyle D, Perumal R, Pokharel M, Oumarou H, Jagadish SVK (2020) Deterioration of ovary plays a key role in heat stress-induced spikelet sterility in sorghum. Plant Cell Environ 43:448–462. https://doi.org/10.1111/pce.13673
Dat J, Vandenabeele S, Vranova E, Montagu MV, Inze D, Breusegem FV (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795. https://doi.org/10.1007/s000180050041
Dhatt BK, Abshire N, Paul P, Hasanthika K, Sandhu J, Zhang Q, Obata T, Walia H (2019) Metabolic dynamics of developing rice seeds under high night-time temperature stress. Front Plant Sci 10:1443. https://doi.org/10.3389/fpls.2019.01443
Djanaguiraman M, Perumal R, Jagadish SVK, Ciampitti IA, Welti R, Prasad PVV (2018a) Sensitivity of sorghum pollen and pistil to high-temperature stress. Plant Cell Environ 41(5):1065–1082. https://doi.org/10.1111/pce.13089
Djanaguiraman M, Perumal R, Ciampitti IA, Gupta SK, Prasad PVV (2018b) Quantifying pearl millet response to high temperature stress: thresholds, sensitive stages, genetic variability and relative sensitivity of pollen and pistil. Plant Cell Environ 41(5):993–1007. https://doi.org/10.1111/pce.12931
Du H, Wang Z, Yu W, Liu W, Huang B (2011) Differential metabolic responses of perennial grass Cynodon transvaalensis X Cynodon dactylon (C4) and Poa pratensis (C3) to heat stress. Physiol Plant 141(3):251–264. https://doi.org/10.1111/j.1399-3054.2010.01432.x
Dunn WB, Broadhurst D, Begley P, Zelena E, Francis-McIntyre S, Anderson N, Brown M, Knowles JD, Halsall A, Haselden JN, Nicholls AW (2011) Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc 6(7):1060–1083. https://doi.org/10.1038/nprot.2011.335
Endo M, Tsuchiya T, Hamada K, Kawamura S, Yano K, Ohshima M, Higashitani A, Watanabe M, Kawagishi-Kobayashi M (2009) High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol 50(11):1911–1922. https://doi.org/10.1093/pcp/pcp135
Guo R, Yang Z, Li F, Yan C, Zhong X, Liu Q, Xia X, Li H, Zhao L (2015) Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol 15(1):1–13. https://doi.org/10.1186/s12870-015-0546-x
Hasegawa T, Kuwagata T, Nishimori M, Ishigooka Y, Murakami M, Yoshimoto M, Kondo M, Ishimaru T, Sawano S, Masaki Y, Matsuzaki H (2009) Recent warming trends and rice growth and yield in Japan. In MARCO symposium on crop production under heat stress: monitoring, impact assessment and adaptation. National Institute for Agro-Environmental Studies, Tsukuba
Herrero M, Hormaza JI (1996) Pistil strategies controlling pollen tube growth. Sex Plant Reprod 9(6):343–347. https://doi.org/10.1007/BF02441953
Hörandl E, Hadacek F (2013) The oxidative damage initiation hypothesis for meiosis. Plant Reprod 26:351–367. https://doi.org/10.1007/s00497-013-0234-7
Hu L, Zhang Z, Xiang Z, Yang Z (2016) Exogenous application of citric acid ameliorates the adverse effect of heat stress in tall fescue (Lolium arundinaceum). Front Plant Sci 7:179. https://doi.org/10.3389/fpls.2016.00179
IPCC (2014) Climate change 2014: synthesis report. In: Pachauri RK, Meyer LA (eds) Contribution of Working Groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. Core Writing Team, IPCC, Geneva
Iqbal N, Fatma M, Khan NA, Umar S (2019) Regulatory role of proline in heat stress tolerance: modulation by salicylic acid. In: Plant Signaling Molecules. Woodhead Publishing, pp 437–448
Ishimaru T, Xaiyalath S, Nallathambi J, Sathishraj R, Yoshimoto M, Phoudalay L, Samson B, Hasegawa T, Hayashi K, Arumugam G, Muthurajan R, Jagadish SVK (2016) Quantifying rice spikelet sterility in potential heat-vulnerable regions: field surveys in Laos and southern India. Field Crops Res 190:3–9. https://doi.org/10.1016/j.fcr.2015.08.006
Iwahori S (1966) High temperature injuries in tomato. V. Fertilization and development of embryo with special reference to the abnormalities caused by high temperature. J Jpn Soc Hortic Sci 35:55–62. https://doi.org/10.2503/jjshs.35.379
Jagadish SVK (2020) Heat stress during flowering in cereals-effects and adaptation strategies. New Phytol 226(6):1567–1572. https://doi.org/10.1111/nph.16429
Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot 61(1):143–156. https://doi.org/10.1093/jxb/erp289
Jagadish SVK, Craufurd PQ, Shi W, Oane R (2014) A phenotypic marker for quantifying heat stress impact during microsporogenesis in rice (Oryza sativa). Funct Plant Biol 41(1):48–55. https://doi.org/10.1071/FP13086
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 Environ 42(1):354–372. https://doi.org/10.1111/pce.13427
Kolupaev Y, Yastreb TO, Karpets YV, Miroshnichenko NN (2011) Influence of salicylic and succinic acids on antioxidant enzymes activity, heat resistance and productivity of Panicum miliaceum L. J Stress Physiol Biochem 7(2):154–163
Kusano M, Fukushima A, Arita M, Jonsson P, Moritz T, Kobayashi M, Hayashi N, Tohge T, Saito K (2007) Unbiased characterization of genotype- dependent metabolic regulations by metabolomic approach in Arabidopsis thaliana. BMC Syst Biol 1:53. https://doi.org/10.1186/1752-0509-1-53
Landschutzel V, Willmitzer L, Muller-Rober B (1995) Inhibition of flower formation by antisense repression of mitochondrial citrate synthase in transgenic potato plants leads to a specific disintegration of the ovary tissues of flowers. EMBO J 14:660–666. https://doi.org/10.1002/j.1460-2075.1995.tb07044.x
Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128(2):682–695. https://doi.org/10.1104/pp.010320
Li X, Lawas LM, Malo R, Glaubitz U, Erban A, Mauleon R, Heuer S, Zuther E, Kopka J, Hincha DK, Jagadish SVK (2015) Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress. Plant Cell Environ 38(10):2171–2192. https://doi.org/10.1111/pce.12545
Lohani N, Singh MB, Bhalla PL (2020) High temperature susceptibility of sexual reproduction in crop plants. J Exp Bot 71(2):555–568. https://doi.org/10.1093/jxb/erz426
Lv Z, Zhu Y, Liu X, Ye H, Tian Y, Li F (2018) Climate change impacts on regional rice production in China. Clim Change 147(3):523–537. https://doi.org/10.1007/s10584-018-2151-0
Mattioli R, Biancucci M, Lonoce C, Costantino P, Trovato M (2012) Proline is required for male gametophyte development in Arabidopsis. BMC Plant Biol 12:236. https://doi.org/10.1186/1471-2229-12-236
Mayer RR, Cherry JH, Rhodes D (1990) Effects of heat shock on amino acid metabolism of cowpea cells. Plant Physiol 94(2):796–810. https://doi.org/10.1104/pp.94.2.796
Polowick PL, Sawhney VK (1988) High temperature induced male and female sterility in canola (Brassica napus L.). Ann Bot 62(1):83–86. https://doi.org/10.1093/oxfordjournals.aob.a087639
Prasad PVV, Bheemanahalli R, Jagadish SVK (2017) Field crops and the fear of heat stress opportunities, challenges, and future directions. Field Crops Res 200:114–121. https://doi.org/10.1016/j.fcr.2016.09.024
Qu M, Chen G, Bunce JA, Zhu X, Sicher RC (2018) Systematic biology analysis on photosynthetic carbon metabolism of maize leaf following sudden heat shock under elevated CO2. Sci Rep 8:7849. https://doi.org/10.1038/s41598-018-26283-x
Razzaq A, Sadia B, Raza A, Hameed KM, Saleem F (2019) Metabolomics: a way forward for crop improvement. Metabolites 9(12):303. https://doi.org/10.3390/metabo9120303
Sage TL, Bagha S, Lundsgaard-Nielsen V, Branch HA, Sultmanis S, Sage RF (2015) The effect of high temperature stress on male and female reproduction in plants. Field Crops Res 182:30–42. https://doi.org/10.1016/j.fcr.2015.06.011
Saini HS, Sedgley M, Aspinall D (1983) Effect of heat stress during floral development on pollen tube growth and ovary anatomy in wheat (Triticum aestivum L.). Funct Plant Biol 10(2):137–144. https://doi.org/10.1071/PP9830137
Satake T, Yoshida S (1978) High temperature-induced sterility in indica rices at flowering. Jpn J Crop Sci 47(1):6–17. https://doi.org/10.1626/jcs.47.6
Sebastiani M, Giordano C, Nediani C, Travaglini C, Borchi E, Zani M, Feccia M, Mancini M, Petrozza V, Cossarizza A, Gallo P, Taylor RW, d’Amati G (2007) Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. J Am Coll Cardiol 50:1362–1369. https://doi.org/10.1016/j.jacc.2007.06.035
Serrano N, Ling Y, Bahieldin A, Mahfouz MM (2019) Thermopriming reprograms metabolic homeostasis to confer heat tolerance. Sci Rep 9(1):1–14. https://doi.org/10.1038/s41598-018-36484-z
Shahid MQ, Sun J, Wei C, Zhang P, Liu X (2010) Studies on the abnormality of embryo sac and pollen fertility in autotetraploid rice during different growing seasons. Pak J Bot 42(1):7–19
Sharma B, Bhatla SC (2013) Accumulation and scavenging of reactive oxygen species and nitric oxide correlate with stigma maturation and pollen–stigma interaction in sunflower. Acta Physiol Plant 35(9):2777–2787. https://doi.org/10.1007/s11738-013-1310-1
Shi W, Li X, Schmidt RC, Struik PC, Yin X, Jagadish SVK (2018) Pollen germination and in vivo fertilization in response to high temperature during flowering in hybrid and inbred rice. Plant Cell Environ 41(6):1287–1297. https://doi.org/10.1111/pce.13146
Shrestha B (2020) Single-cell metabolomics by mass spectrometry. In: Shrestha B (ed) Single cell metabolism methods in molecular biology, vol 2064. Humana, New York. https://doi.org/10.1007/978-1-4939-9831-9_1
Snider JL, Oosterhuis DM, Skulman BW, Kawakami EM (2009) Heat stress-induced limitations to reproductive success in Gossypium hirsutum. Physiol Plant 137(2):125–138. https://doi.org/10.1111/j.1399-3054.2009.01266.x
Snider JL, Oosterhuis DM, Kawakami EM (2011) Mechanisms of reproductive thermotolerance in Gossypium hirsutum: the effect of genotype and exogenous calcium application. J Agron Crop Sci 197(3):228–236. https://doi.org/10.1111/j.1439-037X.2010.00457.x
Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97. https://doi.org/10.1016/j.tplants.2009.11.009
van Oort PA, Zwart SJ (2018) Impacts of climate change on rice production in Africa and causes of simulated yield changes. Glob Chang Biol 24(3):1029–1045. https://doi.org/10.1111/gcb.13967
Vogel E, Donat MG, Alexander LV, Meinshausen M, Ray DK, Karoly D, Meinshausen N, Frieler K (2019) The effects of climate extremes on global agricultural yields. Environ Res Lett 14(5):054010. https://doi.org/10.1088/1748-9326/ab154b
Wang J, Yuan B, Xu Y, Huang B (2018) Differential responses of amino acids and soluble proteins to heat stress associated with genetic variations in heat tolerance for hard fescue. J Am Soc Hortic Sci 143(1):45–55. https://doi.org/10.21273/JASHS04246-17
Wang Y, Impa SM, Sunkar R, Jagadish SVK (2021) The neglected other half-role of the pistil in plant heat stress responses. Plant Cell Environ 44(7):2200–2210. https://doi.org/10.1111/pce.14067
Yan H, Pan X, Chen J, Yao Y, Lu B, Tian X (2015) Out- crossing seed setting rate was seriously reduced by high-temperature in hybrid rice seed production under field conditions. Chin J Rice Sci 29:106–110
Yan H, Zhang B, Zhang Y, Chen X, Xiong H, Matsui T, Tian X (2017) High temperature induced glume closure resulted in lower fertility in hybrid rice seed production. Front Plant Sci 7:1960
Yu J, Du H, Xu M, Huang B (2012) Metabolic responses to heat stress under elevated atmospheric CO2 concentration in a cool-season grass species. J Am Soc Hortic Sci 137(4):221–228
Zeng Y, Hu C, Lu Y, Li J, Liu X (2007) Diversity of abnormal embryo sacs in indica/japonica hybrids in rice demonstrated by confocal microscopy of ovaries. Plant Breed 126(6):574–580. https://doi.org/10.1111/j.1439-0523.2007.01380.x
Zeng YX, Hu CY, Lu YG, Li JQ, Liu XD (2009) Abnormalities occurring during female gametophyte development result in the diversity of abnormal embryo sacs and leads to abnormal fertilization in indica/japonica hybrids in rice. J Integr Plant Biol 51(1):3–12. https://doi.org/10.1111/j.1744-7909.2008.00733.x
Zhang L, Ferguson L, Whiting MD (2018) Temperature effects on pistil viability and fruit set in sweet cherry. Sci Hortic 241:8–17. https://doi.org/10.1016/j.scienta.2018.06.039
Zhao Q, Zhou L, Liu J, Du X, Huang F, Pan G, Cheng F (2018) Relationship of ROS accumulation and superoxide dismutase isozymes in developing anther with floret fertility of rice under heat stress. Plant Physiol Biochem 122:90–101. https://doi.org/10.1016/j.plaphy.2017.11.009
Zinta G, Khan A, AbdElgawad H, Verma V, Srivastava AK (2016) Unveiling the redox control of plant reproductive development during abiotic stress. Front Plant Sci 7:700. https://doi.org/10.3389/fpls.2016.00700