ROS signaling and its involvement in abiotic stress with emphasis on heat stress-driven anther sterility in plants

Abstract

With global warming, crop plants are challenged by heat stress during reproductive growth, leading to male sterility and yield reduction. The balance between reactive oxygen species (ROS) generation and scavenging is disrupted by stress, resulting in oxidative stress which is harmful to crop growth. However, recent advances have shown that ROS signaling via proteins that sense the redox state is positive for plant performance under stress. ROS signaling is also involved in regulating anther development, such as timely tapetum degeneration. We summarize recent progress in uncovering the mechanism of heat stress effects on ROS homeostasis and discuss the relationship between oxidative stress and metabolic disorder, which is often observed during anther development under heat stress. We propose experimental and breeding strategies to improve field crop tolerance to heat stress.

Keywords

Anther development / Crop plants / Heat stress / Heat tolerance strategies / Reactive oxygen species

References

[1] Abouelsaad I., Renault S., 2018. Enhanced oxidative stress in the jasmonic aciddeficient tomato mutant def-1 exposed to NaCl stress. J. Plant Physiol. 226, 136-144.
[2] Al-Zahrani H.S., Alharby H.F., Fahad S., 2022. Antioxidative defense system, hormones, and metabolite accumulation in different plant parts of two contrasting rice cultivars as influenced by plant growth regulators under heat stress. Front. Plant Sci. 13, 911846.
[3] Andrási N., Rigó G., Zsigmond L., Pérez-Salamó I., Papdi C., Klement E., Pettkó- Szandtner A., Baba A.I., Ayaydin F., Dasari R., Cséplő Á., Szabados L., 2019. The mitogen-activated protein kinase 4-phosphorylated heat shock factor A4A regulates responses to combined salt and heat stresses. J. Exp. Bot. 70, 4903-4918.
[4] Babbar R., Karpinska B., Grover A., Foyer C.H., 2021. Heat-induced oxidation of the nuclei and cytosol. Front. Plant Sci. 11, 617779.
[5] Bai W., Wang P., Hong J., Kong W., Xiao Y., Yu X., Zheng H., You S., Lu J., Lei D., Wang C., Wang Q., Liu S., Liu X., Tian Y., Chen L., Jiang L., Zhao Z., Wu C., Wan J., 2019. Earlier Degraded Tapetum1 (EDT1) encodes an ATP-Citrate Lyase required for tapetum programmed cell death. Plant Physiol. 181, 1223-1238.
[6] Baxter C.J., Redestig H., Schauer N., Repsilber D., Patil K.R., Nielsen J., Selbig J., Liu J., Fernie A.R., Sweetlove L.J., 2007. The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol. 143, 312-325.
[7] Begcy K., Nosenko T., Zhou L.Z., Fragner L., Weckwerth W., Dresselhaus T., 2019. Male sterility in maize after transient heat stress during the tetrad stage of pollen development. Plant Physiol. 181, 683-700.
[8] Blokhina O., Fagerstedt K.V., 2010. Oxidative metabolism, ROS and NO under oxygen deprivation. Plant Physiol. Biochem. 48, 359-373.
[9] Borovik O.A., Grabelnych O.I., 2018. Mitochondrial alternative cyanide-resistant oxidase is involved in an increase of heat stress tolerance in spring wheat. J. Plant Physiol. 231, 310-317.
[10] Caliandro R., Nagel K.A., Kastenholz B., Bassi R., Li Z., Niyogi K.K., Pogson B.J., Schurr U., Matsubara S., 2013. Effects of altered α- and β-branch carotenoid biosynthesis on photoprotection and whole-plant acclimation of Arabidopsis to photooxidative stress. Plant Cell Environ. 36, 438-453.
[11] Chapman J.M., Muhlemann J.K., Gayomba S.R., Muday G.K., 2019. RBOH-dependent ROS synthesis and ROS scavenging by plant specialized metabolites to modulate plant development and stress responses. Chem. Res. Toxicol. 32, 370-396.
[12] Chaturvedi P., Wiese A.J., Ghatak A., Zaveska Drabkova L., Weckwerth W., Honys D., 2021. Heat stress response mechanisms in pollen development. New Phytol. 231, 571-585.
[13] Chen L., Wang Q., Tang M., Zhang X., Pan Y., Yang X., Gao G., Lv R., Tao W., Jiang L., Liang T., 2021. QTL mapping and identification of candidate genes for heat tolerance at the flowering stage in rice. Front. Genet. 11, 621871.
[14] Chen Z.S., Liu X.F., Wang D.H., Chen R., Zhang X.L., Xu Z.H., Bai S.N., 2018. Transcription factor OsTGA10 is a target of the MADS protein OsMADS8 and is required for tapetum development. Plant Physiol. 176, 819-835.
[15] Cheng Z., Guo X., Zhang J., Liu Y., Wang B., Li H., Lu H., 2020. βVPE is involved in tapetal degradation and pollen development by activating proprotease maturation in Arabidopsis thaliana. J. Exp. Bot. 71, 1943-1955.
[16] Conrath U., Beckers G.J., Langenbach C.J., Jaskiewicz M.R., 2015. Priming for enhanced defense. Annu. Rev. Phytopathol. 53, 97-119.
[17] Cox D.T.C., Maclean I.M.D., Gardner A.S., Gaston K.J., 2020. Global variation in diurnal asymmetry in temperature, cloud cover, specific humidity and precipitation and its association with leaf area index. Glob. Change Biol. 26, 7099-7111.
[18] Cvetkovska M., Vanlerberghe G.C., 2012. Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol. 195, 32-39.
[19] Czarnocka W., Karpiński S., 2018. Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. Free Radic. Biol. Med. 122, 4-20.
[20] Dai X., Han H., Huang W., Zhao L., Song M., Cao X., Liu C., Niu X., Lang Z., Ma C., Xie H., 2022. Generating novel male sterile tomatoes by editing respiratory burst oxidase homolog genes. Front. Plant Sci. 12, 817101.
[21] Daloso D.M., Müller K., Obata T., Florian A., Tohge T., Bottcher A., Riondet C., Bariat L., Carrari F., Nunes-Nesi A., Buchanan B.B., Reichheld J.P., Araújo W.L., Fernie A.R., 2015. Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria. Proc. Natl. Acad. Sci. U. S. A. 112, 1392-1400.
[22] Ding Y., Fromm M., Avramova Z., 2012. Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat. Commun. 3, 740.
[23] Drerup M.M., Schlücking K., Hashimoto K., Manishankar P., Steinhorst L., Kuchitsu K., Kudla J., 2013. The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol. Plant 6, 559-569.
[24] Dubiella U., Seybold H., Durian G., Komander E., Lassig R., Witte C.P., Schulze W.X., Romeis T., 2013. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. U. S. A. 110, 8744-8749.
[25] Dumont S., Rivoal J., 2019. Consequences of oxidative stress on plant glycolytic and respiratory metabolism. Front. Plant Sci. 10, 166.
[26] Farooq M.A., Niazi A.K., Akhtar J., Saifullah, Farooq M., Souri Z., Karimi N., Rengel Z., 2019. Acquiring control: The evolution of ROS-induced oxidative stress and redox signaling pathways in plant stress responses. Plant Physiol. Biochem. 141, 353-369.
[27] Felemban A., Braguy J., Zurbriggen M.D., Al-Babili S., 2019. Apocarotenoids involved in plant development and stress response. Front. Plant Sci. 10, 1168.
[28] Fu C., Khan M.N., Yan J., Hong X., Zhao F., Chen L., Ma H., Li Y., Li J., Wu H., 2023. Mechanisms of nanomaterials for improving plant salt tolerance. Crop Environ. 2,92-99.
[29] Gao F., Han X., Wu J., Zheng S., Shang Z., Sun D., Zhou R., Li B., 2012. A heat-activated calcium-permeable channel-Arabidopsis cyclic nucleotide-gated ion channel 6-is involved in heat shock responses. Plant J. 70, 1056-1069.
[30] Giesguth M., Sahm A., Simon S., Dietz K.J., 2015. Redox-dependent translocation of the heat shock transcription factor AtHSFA8 from the cytosol to the nucleus in Arabidopsis thaliana. FEBS Lett. 589, 718-725.
[31] Gill S.S., Tuteja N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909-930.
[32] Gómez M.D., Beltrán J.P., Cañas L.A., 2004. The pea END1 promoter drives antherspecific gene expression in different plant species. Planta 219, 967-981.
[33] Gulev S.K., Thorne P.W., Ahn J., Dentener F.J., Domingues C.M., Gerland S., Gong D., Kaufman D.S., Nnamchi H.C., Quaas J., Rivera J.A., Sathyendranath S., Smith S.L., Trewin B., von Schuckmann, K., Vose, R.S., 2021. Changing state of the climate system. In: Masson-Delmotte, V., Zhai, P., Pirani, A., Connors, S.L., Péan, C., Berger, S., Caud, N., Chen, Y., Goldfarb, L., Gomis, M.I., Huang, M., Leitzell, K., Lonnoy, E., Matthews, J.B.R., Maycock, T.K., Waterfield, T., Yelekçi, O., Yu, R., Zhou, B. (Eds.), Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK and New York, USA, pp. 287-422.
[34] Guo C., Chen Y., Wang M., Du Y., Wu D., Chu J., Yao X., 2022. Exogenous brassinolide improves the antioxidant capacity of Pinellia ternata by enhancing the enzymatic and nonenzymatic defense systems under non-stress conditions. Front. Plant Sci. 13, 917301.
[35] Hamza R., Roque E., Gomez-Mena C., Madueno F., Beltran J.P., Cañas L.A., 2021. PsEND1 is a key player in pea pollen development through the modulation of redox homeostasis. Front. Plant Sci. 12, 765277.
[36] Han J.P., Köster, P., Drerup M.M., Scholz M., Li S., Edel K.H., Hashimoto K., Kuchitsu K., Hippler M., Kudla J., 2019. Fine-tuning of RBOHF activity is achieved by differential phosphorylation and Ca²+ binding. New Phytol. 221, 1935-1949.
[37] Hernández I., Alegre L., Van Breusegem F., Munné-Bosch S., 2008. How relevant are flavonoids as antioxidants in plants? Trends Plant Sci. 14, 125-132.
[38] Hilker M., Schwachtje J., Baier M., Balazadeh S., B€aurle I., Geiselhardt S., Hincha D.K., Kunze R., Mueller-Roeber B., Rillig M.C., Rolff J., Romeis T., Schmülling T., Steppuhn A., van Dongen J., Whitcomb S.J., Wurst S., Zuther E., Kopka J., 2016. Priming and memory of stress responses in organisms lacking a nervous system. Biol. Rev. 91, 1118-1133.
[39] Hou L., Zhao M., Huang C., He Q., Zhang L., Zhang J., 2021. Alternative oxidase gene induced by nitric oxide is involved in the regulation of ROS and enhances the resistance of Pleurotus ostreatus to heat stress. Microb. Cell Fact. 20, 137.
[40] Hou X., Rivers J., León P., McQuinn R.P., Pogson B.J., 2016. Synthesis and function of apocarotenoid signals in plants. Trends Plant Sci. 21, 792-803.
[41] Hu C.H., Wang P.Q., Zhang P.P., Nie X.M., Li B.B., Tai L., Liu W.T., Li W.Q., Chen K.M., 2020a. NADPH oxidases: the vital performers and center hubs during plant growth and signaling. Cells 9, 437.
[42] Hu C.H., Zeng Q.D., Tai L., Li B.B., Zhang P.P., Nie X.M., Wang P.Q., Liu W.T., Li W.Q., Kang Z.S., Han D.J., Chen K.M., 2020b. Interaction between TaNOX7 and TaCDPK13 contributes to plant fertility and drought tolerance by regulating ROS production. J. Agric. Food Chem. 68, 7333-7347.
[43] 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.
[44] Hu X., Liu R., Li Y., Wang W., Tai F., Xue R., Li C., 2009. Heat shock protein 70 regulates the abscisic acid-induced antioxidant response of maize to combined drought and heat stress. Plant Growth Regul. 60, 225-235.
[45] Islam M.R., Feng B.H., Chen T.T., Fu W.M., Zhang C.X., Tao L.X., Fu G.F., 2019. Abscisic acid prevents pollen abortion under high-temperature stress by mediating sugar metabolism in rice spikelets. Physiol. Plant. 165, 644-663.
[46] Jacques S., Ghesquiere B., De Bock P.J., Demol H., Wahni K., Willems P., Messens J., Van Breusegem F., Gevaert K., 2015. Protein methionine sulfoxide dynamics in Arabidopsis thaliana under oxidative stress. Mol. Cell. Proteomics 14, 1217-1229.
[47] Jung K.H., Han M.J., Lee Y.S., Kim Y.W., Hwang I., Kim M.J., Kim Y.K., Nahm B.H., An G., 2005. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17, 2705-2722.
[48] Khan A.H., Ma Y., Wu Y., Akbar A., Shaban M., Ullah A., Deng J., Khan A.S., Chi H., Zhu L., Zhang X., Min L., 2023. High-temperature stress suppresses allene oxide cyclase 2 and causes male sterility in cotton by disrupting jasmonic acid signaling. Crop J. 11, 33-45.
[49] Khan A.H., Min L., Ma Y., Wu Y., Ding Y., Li Y., Xie S., Ullah A., Shaban M., Manghwar H., Shahid M., Zhao Y., Wang C., Zhang X., 2020. High day and night temperatures distinctively disrupt fatty acid and jasmonic acid metabolism, inducing male sterility in cotton. J. Exp. Bot. 71, 6128-6141.
[50] Khan A.H., Min L., Ma Y., Zeeshan M., Jin S., Zhang X., 2022. High-temperature stress in crops: male sterility, yield loss and potential remedy approaches. Plant Biotechnol. J. 21, 680-697.
[51] Kim M., Lim J.H., Ahn C.S., Park K., Kim G.T., Kim W.T., Pai H.S., 2006. Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18, 2341-2355.
[52] Kimura S., Hunter K., Vaahtera L., Tran H.C., Citterico M., Vaattovaara A., Rokka A., Stolze S.C., Harzen A., Meissner L., Wilkens M.M.T., Hamann T., Toyota M., Nakagami H., Wrzaczek M., 2020. CRK2 and C-terminal phosphorylation of NADPH oxidase RBOHD regulate reactive oxygen species production in Arabidopsis. Plant Cell 32, 1063-1080.
[53] Kirilovsky D., Kerfeld C.A., 2016. Cyanobacterial photoprotection by the orange carotenoid protein. Nat. Plants 2, 16180.
[54] Ko S.S., Li M.J., Ku M.S.B., Ho Y.C., Lin Y.J., Chuang M.H., Hsing H.X., Lien Y.C., Yang H.T., Chang H.C., Chan M.T., 2014. The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell 26, 2486-2504.
[55] Kobayashi M., Ohura I., Kawakita K., Yokota N., Fujiwara M., Shimamoto K., Doke N., Yoshioka H., 2007. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19, 1065-1080.
[56] Lee E.S., Park J.H., Wi S.D., Kang C.H., Chi Y.H., Chae H.B., Paeng S.K., Ji M.G., Kim W.Y., Kim M.G., Yun D.J., Stacey G., Lee S.Y., 2021. Redox-dependent structural switch and CBF activation confer freezing tolerance in plants. Nat. Plants 7, 914-922.
[57] Lee S., Seo P.J., Lee H.J., Park C.M., 2012. A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J. 70, 831-844.
[58] Li N., Zhang D.S., Liu H.S., Yin C.S., Li X.X., Liang W.Q., Yuan Z., Xu B., Chu H.W., Wang J., Wen T.Q., Huang H., Luo D., Ma H., Zhang D.B., 2006. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999-3014.
[59] Li X.M., Chao D.Y., Wu Y., Huang X., Chen K., Cui L.G., Su L., Ye W.W., Chen H., Chen H.C., Dong N.Q., Guo T., Shi M., Feng Q., Zhang P., Han B., Shan J.X., Gao J.P., Lin H.X., 2015. Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat. Genet. 47, 827-833.
[60] Li Y., Chen M., Khan A.H., Ma Y., He X., Yang J., Zhang R., Ma H., Zuo C., Li Y., Kong J., Wang M., Zhu L., Zhang X., Min L., 2023. Histone H3 lysine 27 trimethylation suppresses jasmonate biosynthesis and signaling to affect male fertility under high temperature in cotton. Plant Commun. 4, 100660.
[61] Li Z., Yue H., Xing D., 2012. MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytol. 195, 85-86.
[62] Liao C., Zheng Y., Guo Y., 2017. MYB30 transcription factor regulates oxidative and heat stress responses through ANNEXIN-mediated cytosolic calcium signaling in Arabidopsis. New Phytol. 216, 163-177.
[63] Lin S., Liu Z., Sun S., Xue F., Li H., Tursun A., Cao L., Zhang L., Wilson Z.A., Zhang D., Liang W., 2023a. Rice HEAT SHOCK PROTEIN60-3B maintains male fertility under high temperature by starch granule biogenesis. Plant Physiol. 192, 2301-2317.
[64] Lin Y., Zhu Y., Cui Y., Qian H., Yuan Q., Chen R., Lin Y., Chen J., Zhou X., Shi C., He H., Hu T., Gu C., Yu X., Zhu X., Wang Y., Qian Q., Zhang C., Wang F., Shang L., 2023b. Identification of natural allelic variation in TTL1 controlling thermotolerance and grain size by a rice super pan-genome. J. Integr. Plant Biol. 65, 2541-2551.
[65] Liu C., Lin J.Z., Wang Y., Tian Y., Zheng H.P., Zhou Z.K., Zhou Y.B., Tang X.D., Zhao X.H., Wu T., Xu S.L., Tang D.Y., Zuo Z.C., He H., Bai L.Y., Yang Y.Z., Liu X.M., 2023. The protein phosphatase PC1 dephosphorylates and deactivates CatC to negatively regulate H₂O₂ homeostasis and salt tolerance in rice. Plant Cell 35, 3604-3625.
[66] Liu D., Li Y.Y., Zhou Z.C., Xiang X., Liu X., Wang J., Hu Z.R., Xiang S.P., Li W., Xiao Q.Z., Wang Y., Hu R.S., Zhao Q., 2021a. Tobacco transcription factor bHLH123 improves salt tolerance by activating NADPH oxidase NtRbohE expression. Plant Physiol. 186, 1706-1720.
[67] Liu S., Li Z., Wu S., Wan X., 2021b. The essential roles of sugar metabolism for pollen development and male fertility in plants. Crop J. 9, 1223-1236.
[68] Luo D., Xu H., Liu Z., Guo J., Li H., Chen L., Fang C., Zhang Q., Bai M., Yao N., Wu H., Wu H., Ji C., Zheng H., Chen Y., Ye S., Li X., Zhao X., Li R., Liu Y.G., 2013. A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat. Genet. 45, 573-577.
[69] Ma L., Jiang H., Ren Y.Y., Yang J.W., Han Y., Si H.J., Prusky D., Bi Y., Wang Y., 2022. Overexpression of StCDPK23 promotes wound healing of potato tubers by regulating StRbohs. Plant Physiol. Biochem. 185, 279-289.
[70] Ma L., Zhang H., Sun L., Jiao Y., Zhang G., Miao C., Hao F., 2012. NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Nat/Kthomeostasis in Arabidopsis under salt stress. J. Exp. Bot. 63, 305-317.
[71] Ma Y., Min L., Wang J., Li Y., Wu Y., Hu Q., Ding Y., Wang M., Liang Y., Gong Z., Xie S., Su X., Wang C., Zhao Y., Fang Q., Li Y., Chi H., Chen M., Khan A.H., Lindsey K., Zhu L., Li X., Zhang X., 2021. A combination of genome-wide and transcriptome-wide association studies reveals genetic elements leading to male sterility during high temperature stress in cotton. New Phytol. 231, 165-181.
[72] Ma Y., Min L., Wang M., Wang C., Zhao Y., Li Y., Fang Q., Wu Y., Xie S., Ding Y., Su X., Hu Q., Zhang Q., Li X., Zhang X., 2018. Disrupted genome methylation in response to high temperature has distinct affects on microspore abortion and anther indehiscence. Plant Cell 30, 1387-1403.
[73] Marino D., Dunand C., Puppo A., Pauly N., 2012. A burst of plant NADPH oxidases. Trends Plant Sci. 17, 9-15.
[74] Maruta T., Inoue T., Tamoi M., Yabuta Y., Yoshimura K., Ishikawa T., Shigeoka S., 2011. Arabidopsis NADPH oxidases, AtrbohD and AtrbohF, are essential for jasmonic acid-induced expression of genes regulated by MYC2 transcription factor. Plant Sci. 180, 655-660.
[75] Masoomi-Aladizgeh F., Najeeb U., Hamzelou S., Pascovici D., Amirkhani A., Tan D.K.Y., Mirzaei M., Haynes P.A., Atwell B.J., 2020. Pollen development in cotton (Gossypium hirsutum) is highly sensitive to heat exposure during the tetrad stage. Plant Cell Environ. 44, 2150-2166.
[76] Maxwell D.P., Wang Y., McIntosh L., 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. U. S. A. 96, 8271-8276.
[77] McLain A.L., Szweda P.A., Szweda L.I., 2011. ɑ-Ketoglutarate dehydrogenase: A mitochondrial redox sensor. Free Radic. Res. 45, 29-36.
[78] Min L., Li Y., Hu Q., Zhu L., Gao W., Wu Y., Ding Y., Liu S., Yang X., Zhang X., 2014. Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton. Plant Physiol. 164, 1293-1308.
[79] Min L., Zhu L., Tu L., Deng F., Yuan D., Zhang X., 2013. Cotton GhCKI disrupts normal male reproduction by delaying tapetum programmed cell death via inactivating starch synthase. Plant J. 75, 823-835.
[80] Mittler R.,2017. ROS are good. Trends Plant Sci. 22, 11-19.
[81] Mittler R., Zandalinas S.I., Fichman Y., Van Breusegem F., 2022. Reactive oxygen species signalling in plant stress responses. Nat. Rev. Mol. Cell Biol. 23, 663-679.
[82] Møller I.M.,2001. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 561-591.
[83] Muhlemann J.K., Younts T.L.B., Muday G.K., 2018. Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress. Proc. Natl. Acad. Sci. U. S. A. 115, E11188-E11197.
[84] Müller F., Rieu I., 2016. Acclimation to high temperature during pollen development. Plant Reprod. 29, 107-118.
[85] Murphy M.P.,2009. How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13.
[86] Narayanan S., Prasad P.V.V., Welti R., 2018. Alterations in wheat pollen lipidome during high day and night temperature stress. Plant Cell Environ. 41, 1749-1761.
[87] Niu N., Liang W., Yang X., Jin W., Wilson Z.A., Hu J., Zhang D., 2013. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat. Commun. 4, 1445.
[88] Paradiso A., Domingo G., Blanco E., Buscaglia A., Fortunato S., Marsoni M., Scarcia P., Caretto S., Vannini C., de Pinto M.C., 2020. Cyclic AMP mediates heat stress response by the control of redox homeostasis and ubiquitin-proteasome system. Plant Cell Environ. 43, 2727-2742.
[89] Pucciariello C., Perata P., 2017. New insights into reactive oxygen species and nitric oxide signalling under low oxygen in plants. Plant Cell Environ. 40, 473-482.
[90] Qiao B., Zhang Q., Liu D., Wang H., Yin J., Wang R., He M., Cui M., Shang Z., Wang D., Zhu Z., 2015. A calcium-binding protein, rice annexin OsANN1, enhances heat stress tolerance by modulating the production of H₂O₂. J. Exp. Bot. 66, 5853-5866.
[91] Rejeb K.B., Lefebvre-De Vos D., Le Disquet I.L., Leprince A.S., Bordenave M., Maldiney R., Jdey A., Abdelly C., Savouré A., 2015. Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol. 208, 1138-1148.
[92] Santiago J.P., Soltani A., Bresson M.M., Preiser A.L., Lowry D.B., Sharkey T.D., 2021. Contrasting anther glucose-6-phosphate dehydrogenase activities between two bean varieties suggest an important role in reproductive heat tolerance. Plant Cell Environ. 44, 2185-2199.
[93] Selinski J., Scheibe R., Day D.A., Whelan J., 2018. Alternative oxidase is positive for plant performance. Trends Plant Sci. 23, 588-597.
[94] Sirichandra C., Gu D., Hu H.C., Davanture M., Lee S., Djaoui M., Valot B., Zivy M., Leung J., Merlot S., Kwak J.M., 2009. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 583, 2982-2986.
[95] Song P., Jia Q., Chen L., Jin X., Xiao X., Li L., Chen H., Qu Y., Su Y., Zhang W., Zhang Q., Vissenberg K., 2020. Involvement of Arabidopsis phospholipase D δ in regulation of ROS-mediated microtubule organization and stomatal movement upon heat shock. J. Exp. Bot. 71, 6555-6570.
[96] Sun M., Jiang F., Zhou R., Wen J., Cui S., Wang W., Wu Z., 2019. Respiratory burst oxidase homologue-dependent H₂O₂ is essential during heat stress memory in heat sensitive tomato. Sci. Hortic. 258, 108777.
[97] Suzuki N., Miller G., Salazar C., Mondal H.A., Shulaev E., Cortes D.F., Shuman J.L., Luo X., Shah J., Schlauch K., Shulaev V., Mittler R., 2013. Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25, 3553-3569.
[98] Ugalde J.M., Fuchs P., Nietzel T., Cutolo E.A., Homagk M., Vothknecht U.C., Holuigue L., Schwarzl€ander M., Müller-Schüssele S.J., Meyer A.J., 2021. Chloroplast-derived photo-oxidative stress causes changes in H₂O₂ and EGSH in other subcellular compartments. Plant Physiol. 186, 125-141.
[99] Van Aken, O., 2021. Mitochondrial redox systems as central hubs in plant metabolism and signaling. Plant Physiol. 186, 36-52.
[100] Viola I.L., Camoirano A., Gonzalez D.H., 2016. Redox-dependent modulation of anthocyanin biosynthesis by the TCP transcription factor TCP15 during exposure to high light intensity conditions in Arabidopsis. Plant Physiol. 170, 74-85.
[101] Wagner S., Steinbeck J., Fuchs P., Lichtenauer S., Els€asser M., Schippers J.H.M., Nietzel T., Ruberti C., Van Aken O., Meyer A.J., Van Dongen J.T., Schmidt R.R., Schwarzl€ander M., 2019. Multiparametric real-time sensing of cytosolic physiology links hypoxia responses to mitochondrial electron transport. New Phytol. 224, 1668-1684.
[102] Wang W., Chen D., Liu D., Cheng Y., Zhang X., Song L., Hu M., Dong J., Shen F., 2020. Comprehensive analysis of the Gossypium hirsutum L. respiratory burst oxidase homolog (Ghrboh) gene family. BMC Genomics 21, 91.
[103] Wang W., Chen D., Zhang X., Liu D., Cheng Y., Shen F., 2018. Role of plant respiratory burst oxidase homologs in stress responses. Free Radic. Res. 52, 826-839.
[104] Wang W., Zhang J., Ai L., Wu D., Li B., Zhang L., Zhao L., 2021. Cyclic nucleotidegated ion channel 6 mediates thermotolerance in Arabidopsis seedlings by regulating hydrogen peroxide production via cytosolic calcium ions. Front. Plant Sci. 12, 708672.
[105] Wang X., Ma X., Wang H., Li B., Clark G., Guo Y., Roux S., Sun D., Tang W., 2015a. Proteomic study of microsomal proteins reveals a key role for Arabidopsis annexin 1 in mediating heat stress-induced increase in intracellular calcium levels. Mol. Cell. Proteomics 14, 686-694.
[106] Wang X., Vignjevic M., Liu F., Jacobsen S., Jiang D., Wollenweber B., 2015b. Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regul. 75, 677-687.
[107] Wang X., Zhang M.M., Wang Y.J., Gao Y.T., Li R., Wang G.F., Li W.Q., Liu W.T., Chen K.M., 2016. The plasma membrane NADPH oxidase OsRbohA plays a crucial role in developmental regulation and drought-stress response in rice. Physiol. Plant. 156, 421-443.
[108] Wong H.L., Pinontoan R., Hayashi K., Tabata R., Yaeno T., Hasegawa K., Kojima C., Yoshioka H., Iba K., Kawasaki T., Shimamoto K., 2007. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19, 4022-4034.
[109] Wu F., Chi Y., Jiang Z., Xu Y., Xie L., Huang F., Wan D., Ni J., Yuan F., Wu X., Zhang Y., Wang L., Ye R., Byeon B., Wang W., Zhang S., Sima M., Chen S., Zhu M., Pei J., Johnson D.M., Zhu S., Cao X., Pei C., Zai Z., Liu Y., Liu T., Swift G.B., Zhang W., Yu M., Hu Z., Siedow J.N., Chen X., Pei Z.M., 2020. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578, 577-581.
[110] Wu H., Li Z., 2022. Recent advances in nano-enabled agriculture for improving plant performance. Crop J. 10, 1-12.
[111] Xiao Y., You S., Kong W., Tang Q., Bai W., Cai Y., Zheng H., Wang C., Jiang L., Wang C., Zhao Z., Wan J., 2019. A GARP transcription factor anther dehiscence defected 1 (OsADD1) regulates rice anther dehiscence. Plant Mol. Biol. 101, 403-414.
[112] Xie H.T., Wan Z.Y., Li S., Zhang Y., 2007-2023.
[113] Xie X., Zhang Z., Zhao Z., Xie Y., Li H., Ma X., Liu Y.G., Chen L., 2020. The mitochondrial aldehyde dehydrogenase OsALDH2b negatively regulates tapetum degeneration in rice. J. Exp. Bot. 71, 2551-2560.
[114] Xiong D., Ling X., Huang J., Peng S., 2017. Meta-analysis and dose-response analysis of high temperature effects on rice yield and quality. Environ. Exp. Bot. 141, 1-9.
[115] Xiong H., Hua L., Reyna-Llorens I., Shi Y., Chen K.M., Smirnoff N., Kromdijk J., Hibberd J.M., 2021. Photosynthesis-independent production of reactive oxygen species in the rice bundle sheath during high light is mediated by NADPH oxidase. Proc. Natl. Acad. Sci. U. S. A. 118, e2022702118.
[116] Yan M.Y., Xie D.L., Cao J.J., Xia X.J., Shi K., Zhou Y.H., Zhou J., Foyer C.H., Yu J.Q., 2020. Brassinosteroid-mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato. Plant J. 102, 931-947.
[117] Yang C., Song J., Ferguson A.C., Klisch D., Simpson K., Mo R., Taylor B., Mitsuda N., Wilson Z.A., 2017. Transcription factor MYB26 is key to spatial specificity in anther secondary thickening formation. Plant Physiol. 175, 333-350.
[118] Yang Z., Sun L., Zhang P., Zhang Y., Yu P., Liu L., Abbas A., Xiang X., Wu W., Zhan X., Cao L., Cheng S., 2019. TDR INTERACTING PROTEIN 3, encoding a PHDfinger transcription factor, regulates Ubisch bodies and pollen wall formation in rice. Plant J. 99, 844-861.
[119] Yao Y., He R.J., Xie Q.L., Zhao X.H., Deng X.M., He J.B., Song L., He J., Marchant A., Chen X.Y., Wu A.M., 2017. ETHYLENE RESPONSE FACTOR 74 (ERF74) plays an essential role in controlling a respiratory burst oxidase homolog D (RbohD)-dependent mechanismin response to different stresses in Arabidopsis. NewPhytol. 213, 1667-1681.
[120] Yi J., Moon S., Lee Y.S., Zhu L., Liang W., Zhang D., Jung K.H., An G., 2016. Defective Tapetum Cell Death 1 (DTC1) regulates ROS levels by binding to metallothionein during tapetum degeneration. Plant Physiol. 170, 1611-1623.
[121] Yu S.X., Feng Q.N., Xie H.T., Li S., Zhang Y., 2017. Reactive oxygen species mediate tapetal programmed cell death in tobacco and tomato. BMC Plant Biol. 17, 76.
[122] Zandalinas S.I., Mittler R., 2021. Vascular and nonvascular transmission of systemic reactive oxygen signals during wounding and heat stress. Plant Physiol. 186, 1721-1733.
[123] Zhang A., Zhang J., Ye N., Cao J., Tan M., Zhang J., Jiang M., 2010. ZmMPK5 is required for theNADPH oxidase-mediated self-propagation of apoplastic H₂O₂ in brassinosteroidinduced antioxidant defence in leaves of maize. J. Exp. Bot. 61, 4399-4411.
[124] Zhang D., Luo X., Zhu L., 2011. Cytological analysis and genetic control of rice anther development. J. Genet. Genomics 38, 379-390.
[125] Zhang M., Li Z., Feng K., Ji Y., Xu Y., Tu D., Teng B., Liu Q., Liu J., Zhou Y., Wu W., 2023. Strategies for indica rice adapted to high-temperature stress in the middle and lower reaches of the Yangtze River. Front. Plant Sci. 13, 1081807.
[126] Zhang W., Sheng J., Xu Y., Xiong F., Wu Y., Wang W., Wang Z., Yang J., Zhang J., 2019. Role of brassinosteroids in rice spikelet differentiation and degeneration under soil-drying during panicle development. BMC Plant Biol. 19, 409.
[127] Zhang X., Zhuang L., Liu Y., Yang Z., Huang B., 2020. Protein phosphorylation associated with drought priming-enhanced heat tolerance in a temperate grass species. Hortic. Res. 7, 207.
[128] Zhao L., Lu L., Wang A., Zhang H., Huang M., Wu H., Xing B., Wang Z., Ji R., 2020. Nano-biotechnology in agriculture: use of nanomaterials to promote plant growth and stress tolerance. J. Agric. Food Chem. 68, 1935-1947.
[129] Zhao Q., Guan X., Zhou L., Asad M.A.U., Xu Y., Pan G., Cheng F., 2023a. ABAtriggered ROS burst in rice developing anthers is critical for tapetal programmed cell death induction and heat stress-induced pollen abortion. Plant Cell Environ. 46, 1453-1471.
[130] Zhao Q., Guan X., Zhou L., Xu Y., Asad M.A.U., Pan G., Cheng F., 2023b. OsPDIL1-1 controls ROS generation by modulating NADPH oxidase in developing anthers to alter the susceptibility of floret fertility to heat for rice. Environ. Exp. Bot. 205, 105103.
[131] Zhao Q., Zhou L., Liu J., Cao Z., Du X., Huang F., Pan G., Cheng F., 2018a. Involvement of CAT in the detoxification of HT-induced ROS burst in rice anther and its relation to pollen fertility. Plant Cell Rep. 37, 741-757.
[132] Zhao Q., Zhou L., Liu J., Du X., Asad M.A., Huang F., Pan G., Cheng F., 2018b. 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.
[133] Zhao Y., Du H., Wang Y., Wang H., Yang S., Li C., Chen N., Yang H., Zhang Y., Zhu Y., Yang L., Hu X., 2021. The calcium-dependent protein kinase ZmCDPK7 functions in heat-stress tolerance in maize. J. Integr. Plant Biol. 63, 510-527.
[134] Zheng S., Li J., Ma L., Wang H., Zhou H., Ni E., Jiang D., Liu Z., Zhuang C., 2019. OsAGO₂ controls ROS production and the initiation of tapetal PCD by epigenetically regulating OsHXK1 express

Funding

* E-mail address: [e-mail] (L. Min).