Hydrogen peroxide mediates high-intensity blue light-induced hypocotyl phototropism of cotton seedlings

Qian-yi Lv, Qing-ping Zhao, Chen Zhu, Meichen Ding, Fang-yuan Chu, Xing-kun Li, Kai Cheng, Xiang Zhao

Stress Biology ›› 2023, Vol. 3 ›› Issue (1) : 27. DOI: 10.1007/s44154-023-00111-3
Original Paper

Hydrogen peroxide mediates high-intensity blue light-induced hypocotyl phototropism of cotton seedlings

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Abstract

Phototropism is a classic adaptive growth response that helps plants to enhance light capture for photosynthesis. It was shown that hydrogen peroxide (H2O2) participates in the regulation of blue light-induced hypocotyl phototropism; however, the underlying mechanism is unclear. In this study, we demonstrate that the unilateral high-intensity blue light (HBL) could induce asymmetric distribution of H2O2 in cotton hypocotyls. Disruption of the HBL-induced asymmetric distribution of H2O2 by applying either H2O2 itself evenly on the hypocotyls or H2O2 scavengers on the lit side of hypocotyls could efficiently inhibit hypocotyl phototropic growth. Consistently, application of H2O2 on the shaded and lit sides of the hypocotyls led to reduced and enhanced hypocotyl phototropism, respectively. Further, we show that H2O2 inhibits hypocotyl elongation of cotton seedlings, thus supporting the repressive role of H2O2 in HBL-induced hypocotyl phototropism. Moreover, our results show that H2O2 interferes with HBL-induced asymmetric distribution of auxin in the cotton hypocotyls. Taken together, our study uncovers that H2O2 changes the asymmetric accumulation of auxin and inhibits hypocotyl cell elongation, thus mediating HBL-induced hypocotyl phototropism.

Keywords

Hydrogen peroxide / High-intensity blue light / Hypocotyl phototropism / Cotton

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Qian-yi Lv, Qing-ping Zhao, Chen Zhu, Meichen Ding, Fang-yuan Chu, Xing-kun Li, Kai Cheng, Xiang Zhao. Hydrogen peroxide mediates high-intensity blue light-induced hypocotyl phototropism of cotton seedlings. Stress Biology, 2023, 3(1): 27 https://doi.org/10.1007/s44154-023-00111-3

References

[1]
ApelK, HirtH. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol, 2004, 55: 373-399
CrossRef Google scholar
[2]
BaoY, HuG, FlagelLE, SalmonA, BezanillaM, PatersonAH, WangZ, WendelJF. Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium). Proc Natl Acad Sci, 2011, 108: 21152-21157
CrossRef Google scholar
[3]
BarbezE, DunserK, GaidoraA, LendlT, BuschW. Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana. Proc Natl Acad Sci, 2017, 114: E4884-E4893
CrossRef Google scholar
[4]
ČernýM, HabánováH, BerkaM, LuklováM, BrzobohatýB. Hydrogen peroxide: its role in plant biology and crosstalk with signalling networks. Int J Mol Sci, 2018, 19: 2812
CrossRef Google scholar
[5]
ChandrakuntalK, KumarPG, LalorayaM, LalorayaMM. Direct involvement of hydrogen peroxide in curvature of wheat coleoptile in blue-light-treated and dark-grown coleoptiles. Biochem Biophys Res Commun, 2004, 319: 1190-1196
CrossRef Google scholar
[6]
ChristieJM. Phototropin blue-light receptors. Annu Rev Plant Biol, 2007, 58: 21-45
CrossRef Google scholar
[7]
ChristieJM, ReymondP, PowellGK, BernasconiP, RaibekasAA, LiscumE, BriggsWR. Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science, 1998, 282: 1698-1701
CrossRef Google scholar
[8]
ChristieJM, YangH, RichterGL, SullivanS, ThomsonCE, LinJ, TitapiwatanakunB, EnnisM, KaiserliE, LeeOR, AdamecJ, PeerWA, MurphyAS. Phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol, 2011, 9: e1001076
CrossRef Google scholar
[9]
DemarsyE, FankhauserC. Higher plants use LOV to perceive blue light. Curr Opin Plant Biol, 2009, 12: 69-74
CrossRef Google scholar
[10]
DemarsyE, SchepensI, OkajimaK, HerschM, BergmannS, ChristieJ, ShimazakiK, TokutomiS, FankhauserC. Phytochrome Kinase Substrate 4 is phosphorylated by the phototropin 1 photoreceptor. EMBO J, 2012, 31: 3457-3467
CrossRef Google scholar
[11]
DingZ, Galvan-AmpudiaCS, DemarsyE, LangowskiL, Kleine-VehnJ, FanY, MoritaMT, TasakaM, FankhauserC, OffringaR, FrimlJ. Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol, 2011, 13: 447-452
CrossRef Google scholar
[12]
FormanHJ, TorresM. Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am J Respir Crit Care Med, 2002, 166: S4-S8
CrossRef Google scholar
[13]
GillSS, TutejaN. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem, 2010, 48: 909-930
CrossRef Google scholar
[14]
GoyalA, SzarzynskaB, FankhauserC. Phototropism: at the crossroads of light-signaling pathways. Trends Plant Sci, 2013, 18: 393-401
CrossRef Google scholar
[15]
GrunewaldW, FrimlJ. The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J, 2010, 29: 2700-2714
CrossRef Google scholar
[16]
HarutaM, SabatG, SteckerK, MinkoffBB, SussmanMR. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science, 2014, 343: 408-411
CrossRef Google scholar
[17]
HenleES, LinnS. Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J Biol Chem, 1997, 272: 19095-19098
CrossRef Google scholar
[18]
HohmT, DemarsyE, QuanC, Allenbach PetrolatiL, PreutenT, VernouxT, BergmannS, FankhauserC. Plasma membrane H+-ATPase regulation is required for auxin gradient formation preceding phototropic growth. Mol Syst Biol, 2014, 10: 751
CrossRef Google scholar
[19]
HollandJJ, RobertsD, LiscumE. Understanding phototropism: from Darwin to today. J Exp Bot, 2009, 60: 1969-1978
CrossRef Google scholar
[20]
InadaS, OhgishiM, MayamaT, OkadaK, SakaiT. RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell, 2004, 16: 887-896
CrossRef Google scholar
[21]
Janicka-RussakM, KabałaK. Abscisic acid and hydrogen peroxide induce modification of plasma membrane H(+)-ATPase from Cucumis sativus L. roots under heat shock. J Plant Physiol, 2012, 169: 1607-1614
CrossRef Google scholar
[22]
JiangZ, ZhuS, YeR, XueY, ChenA, A L, Pei ZM,. Relationship between NaCl- and H2O2-induced cytosolic Ca2+ increases in response to stress in Arabidopsis. Plos One, 2013, 10: e76130
CrossRef Google scholar
[23]
KamiC, AllenbachL, ZourelidouM, LjungK, SchutzF, IsonoE, WatahikiMK, YamamotoKT, SchwechheimerC, FankhauserC. Reduced phototropism in pks mutants may be due to altered auxinregulated gene expression or reduced lateral auxin transport. Plant J, 2014, 77: 393-403
CrossRef Google scholar
[24]
KimuraT, HagaK, NomuraY, HigakiT, NakagamiH, SakaiT. Phosphorylation of NONPHOTOTROPIC HYPOCOTYL3 affects photosensory adaptation during the phototropic response. Plant Physiol, 2021, 187: 981-995
CrossRef Google scholar
[25]
KimuraT, HagaK, SakaiT. The phosphorylation status of NONPHOTOTROPIC HYPOCOTYL3 affects phot2-dependent phototropism in Arabidopsis. Plant Signal Behav, 2022, 17: 2027138
CrossRef Google scholar
[26]
LariguetP, SchepensI, HodgsonD, PedmaleUV, TrevisanM, KamiC, de CarbonnelM, AlonsoJM, EckerJR, LiscumE, FankhauserC. PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1 binding protein required for phototropism. Proc Natl Acad Sci, 2006, 103: 10134-10139
CrossRef Google scholar
[27]
LiC, YehFL, CheungAY, DuanQ, KitaD, LiuMC, MamanJ, LuuEJ, WuBW, GatesL, JalalM, KwongA, CarpenterH, WuHM. Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife, 2015, 4: e06587
CrossRef Google scholar
[28]
LiC, LiuX, QiangX, LiX, LiX, ZhuS, WangL, WangY, LiaoH, LuanS, YuF. EBP1 nuclear accumulation negatively feeds back on FERONIA-mediated RALF1 signaling. PLoS Biol, 2018, 16: e2006340
CrossRef Google scholar
[29]
LiP, CaiQ, WangH, LiS, ChengJ, LiH, YuQ, WuS. Hydrogen peroxide homeostasis provides beneficial micro-environment for SHR-mediated periclinal division in Arabidopsis root. New Phytol, 2020, 228: 1926-1938
CrossRef Google scholar
[30]
LiC, ChenJ, LiX, ZhangX, LiuY, ZhuS, WangL, ZhengH, LuanS, LiJ, YuF. FERONIA is involved in phototropin 1-mediated blue light phototropic growth in Arabidopsis. J Integr Plant Biol, 2022, 64: 1901-1915
CrossRef Google scholar
[31]
LinD, YanR, XingM, LiaoS, ChenJ, GanZ. Fucoidan treatment alleviates chilling injury in cucumber by regulating ROS homeostasis and energy metabolism. Front Plant Sci, 2022, 13: 1107687
CrossRef Google scholar
[32]
LiscumE, BriggsWR. Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. Plant Cell, 1995, 7: 473-485
CrossRef Google scholar
[33]
LiscumE, AskinosieSK, LeuchtmanDL, MorrowJ, WillenburgKT, CoatsDR. Phototropism: growing towards an understanding of plant movement. Plant Cell, 2014, 26: 38-55
CrossRef Google scholar
[34]
Lopez VazquezA, Allenbach PetrolatiL, LegrisM, DessimozC, LampugnaniER, GloverN, FankhauserC. Protein S-acylation controls the subcellular localization and biological activity of phytochrome kinase substrate. Plant Cell, 2023, 35(7):2635-2653
CrossRef Google scholar
[35]
MittlerR. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci, 2002, 7: 405-410
CrossRef Google scholar
[36]
MittlerR, VanderauweraS, SuzukiN, MillerG, TognettiVB, VandepoeleK, GolleryM, ShulaevV, Van BreusegemF. ROS signaling: the new wave?. Trends Plant Sci, 2011, 16: 300-309
CrossRef Google scholar
[37]
MotchoulskiA, LiscumE. Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for phototropism. Science, 1999, 286: 961-964
CrossRef Google scholar
[38]
NazirF, FariduddinQ, KhanTA. Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere, 2020, 252: 126486
CrossRef Google scholar
[39]
NeillS, DesikanR, HancockJ. Hydrogen peroxide signalling. Curr Opin Plant Biol, 2002, 5: 388-395
CrossRef Google scholar
[40]
PengX, ZhangYA, WanCP, GanZY, ChenCY, ChenJY. Antofine triggers the resistance against penicillium italicum in ponkan fruit by driving AsA-GSH cycle and ROS-scavenging system. Front Microbiol, 2022, 13: 874430
CrossRef Google scholar
[41]
RusaczonekA, CzarnockaW, WillemsP, Sujkowska-RybkowskaM, BreusegemFV, Karpiński, . Phototropin 1 and 2 influence photosynthesis, UV-C induced photooxidative stress responses, and cell death. Cell, 2021, 10: 200
CrossRef Google scholar
[42]
SakaiT, WadaT, IshiguroS, OkadaK. RPT2: A signal transducer of the phototropic response in Arabidopsis. Plant Cell, 2000, 12: 225-236
CrossRef Google scholar
[43]
SakaiT, KagawaT, KasaharaM, SwartzTE, ChristieJM, BriggsWR, WadaM, OkadaK. Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci, 2001, 98: 6969-6974
CrossRef Google scholar
[44]
SchumacherP, DemarsyE, WaridelP, PetrolatiLA, TrevisanM, FankhauserC. A phosphorylation switch turns a positive regulator of phototropism into an inhibitor of the process. Nat Commun, 2018, 9: 2403
CrossRef Google scholar
[45]
ShortTW, BriggsWR. Characterization of a rapid, blue light-mediated change in detectable phosphorylation of a plasma membrane protein from etiolated pea (Pisum sativum L.) seedlings. Plant Physiol, 1990, 92: 179-185
CrossRef Google scholar
[46]
SmirnoffN, ArnaudD. Hydrogen peroxide metabolism and functions in plants. New Phytol, 2019, 221: 1197-1214
CrossRef Google scholar
[47]
SullivanS, KharshiingE, LairdJ, SakaiT, ChristieJM. Deetiolation enhances phototropism by modulating NON-PHOTOTROPIC HYPOCOTYL3 phosphorylation status. Plant Physiol, 2019, 180: 1119-1131
CrossRef Google scholar
[48]
TognettiVB, Van AkenO, MorreelK, VandenbrouckeK, van de CotteB, De ClercqI, ChiwochaS, FenskeR, PrinsenE, BoerjanW, GentyB, StubbsKA, InzéD, Van BreusegemF. Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell, 2010, 22: 2660-2679
CrossRef Google scholar
[49]
TsengTS, BriggsWR. The Arabidopsis rcn1-1 mutation impairs dephosphorylation of Phot2, resulting in enhanced blue light responses. Plant Cell, 2010, 22: 392-402
CrossRef Google scholar
[50]
Tsuchida-MayamaT, NakanoM, UeharaU, SanoM, FujisawaN, OkadaK, SakaiT. Mapping of the phosphorylation sites on the phototropic signal transducer, NPH3. Plant Sci, 2008, 174: 626-633
CrossRef Google scholar
[51]
VealE, DayA. Hydrogen peroxide as a signaling molecule. Antioxid Redox Signal, 2011, 15: 147-151
CrossRef Google scholar
[52]
WaksmanT, SuetsuguN, HermanowiczP, RonaldJ, SullivanS, ŁabuzJ, ChristieJM. Phototropin phosphorylation of ROOT PHOTOTROPISM 2 and its role in mediating phototropism, leaf positioning, and chloroplast accumulation movement in Arabidopsis. Plant J, 2023, 114: 390-402
CrossRef Google scholar
[53]
WangX, HanL, YinH, ZhaoZ, CaoH, ShangZ, KangE. AtANN1 and AtANN2 are involved in phototropism of etiolated hypocotyls of Arabidopsis by regulating auxin distribution. AoB Plants, 2012, 14: plab075
CrossRef Google scholar
[54]
WentFW, ThimannKV. Phytohormones, 1937 New York Macmillan Company
[55]
WhippoCW, HangarterRP. Phototropism: bending towards enlightenment. Plant Cell, 2006, 18: 1110-1119
CrossRef Google scholar
[56]
XieQ, EssemineJ, PangX, ChenH, CaiW. Exogenous application of abscisic acid to shoots promotes primary root cell division and elongation. Plant Sci, 2020, 292: 110385
CrossRef Google scholar
[57]
YuanHM, LiuWC, JinY, LuYT. Role of ROS and auxin in plant response to metal-mediated stress. Plant Signal Behav, 2013, 8: e24671
CrossRef Google scholar
[58]
ZhangX, WangH, TakemiyaA, SongCP, KinoshitaT, ShimazakiK. Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts. Plant Physiol, 2004, 136: 4150-4158
CrossRef Google scholar
[59]
ZhangJ, CaiL, ChengJ, MaoH, FanX, MengZ, ChanKM, ZhangH, QiJ, JiL, HongY. Transgene integration and organization in cotton (Gossypium hirsutum L.) genome. Transgenic Res, 2008, 17: 293-306
CrossRef Google scholar
[60]
ZhangY, SunY, LiW, LiJ, XuR, DuJ, LiZ, LiG, YangK. Chelator iminodisuccinic acid regulates Reactive Oxygen species accumulation and improves Maize (Zea mays L.) seed germination under Pb stress. Plants (Basel), 2022, 11: 2487
CrossRef Google scholar
[61]
ZhaoX, WangYL, QiaoXR, WangJ, WangLD, XuCS, ZhangX. Phototropins function in high-intensity blue light-induced hypocotyl phototropism in Arabidopsis by altering cytosolic calcium. Plant Physiol, 2013, 162: 1539-1551
CrossRef Google scholar
[62]
ZhaoQP, ZhuJD, LiNN, WangXN, ZhaoX, ZhangX. Cryptochrome-mediated hypocotyl phototropism was regulated antagonistically by gibberellic acid and sucrose in Arabidopsis. J Integr Plant Biol, 2020, 62: 614-630
CrossRef Google scholar
[63]
ZhouL, HouH, YangT, LianY, SunY, BianZ, WangC. Exogenous hydrogen peroxide inhibits primary root gravitropism by regulating auxin distribution during Arabidopsis seed germination. Plant Physiol Biochem, 2018, 128: 126-133
CrossRef Google scholar
[64]
ZhuJD, WangJ, GuoXN, ShangBS, YanHR, ZhangX, ZhaoX. A high concentration of abscisic acid inhibits hypocotyl phototropism in Gossypium arboreum by reducing accumulation and asymmetric distribution of auxin. J Exp Bot, 2021, 72: 6365-6381
CrossRef Google scholar
Funding
National Natural Science Foundation of ChinaNational Natural Science Foundation of China(32100225); National Natural Science Foundation of China(31871419); Natural Science Foundation of Henan Province(212300410214); Central Plain Talent Scheme(ZYYCYU202012164)

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