Hydrogen peroxide as a systemic messenger in the photosynthetic induction of mulberry leaves

Wei Li , Geng Chen , Yujiao Fang , Tao Wang , Yixiong Wu , Yue Wu , Xinmeng Liu , Baiwen Jiang

Journal of Forestry Research ›› 2020, Vol. 32 ›› Issue (3) : 945 -952.

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Journal of Forestry Research ›› 2020, Vol. 32 ›› Issue (3) : 945 -952. DOI: 10.1007/s11676-020-01165-z
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Hydrogen peroxide as a systemic messenger in the photosynthetic induction of mulberry leaves

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Abstract

Mulberry (Morus alba L.) seedlings were used to test hydrogen peroxide (H2O2) as a potential systemic messenger in photosynthetic induction. The upper leaf of mulberry was dark-adapted for 45 min and then illuminated with photosynthetically active radiation (PAR) of 1000 μmol m−2 s−1. Photosynthetic induction and H2O2 content in the lower leaf was measured. The results show that pre-illumination of the upper leaf promoted photosynthetic induction and increased endogenous H2O2 in the lower leaf. Without pre-illuminating upper leaf, exogenous H2O2 treatment on the lower leaf promoted photosynthetic induction. The application of diphenyleneiodonium and trichloroacetic acid on petioles of the upper leaf inhibited H2O2 increase in the lower leaf, indicating that H2O2 transport was from upper leaves to lower leaves through the phloem. The results show that H2O2 might serve as a signal messenger to promote rapid induction of photosynthesis of leaves in lower parts of the canopy and enable plants to use light energy more efficiently.

Keywords

Hydrogen peroxide / Photosynthetic induction / Mulberry seedlings / Systematic signal / Passway

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Wei Li, Geng Chen, Yujiao Fang, Tao Wang, Yixiong Wu, Yue Wu, Xinmeng Liu, Baiwen Jiang. Hydrogen peroxide as a systemic messenger in the photosynthetic induction of mulberry leaves. Journal of Forestry Research, 2020, 32(3): 945-952 DOI:10.1007/s11676-020-01165-z

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References

[1]

Bai KD, Liao DB, Jiang DB, Cao KF. Photosynthetic induction in leaves of co-occurring Fagus lucida and Castanopsis lamontii saplings grown in contrasting light environments. Trees, 2008, 22(4): 449-462.

[2]

Carmo-Silva AE, Salvucci ME. The regulatory properties of rubisco activase differ among species and affect photosynthetic induction during light transitions. Plant Physiol, 2013, 161(4): 1645-1655.

[3]

Cheng DD, Liu MJ, Sun XB, Zhao M, Chow WS, Sun GY, Zhang ZS, Hu YB. Light suppresses bacterial populations through the accumulation of hydrogen peroxide in tobacco leaves infected with Pseudomonas syringae pv. tabaci. Frontiers in Plant Science, 2016, 7(512): 1-11.

[4]

Cheng YL, Song CP. Hydrogen peroxide homeostasis and signaling in plant cells. Science in China. Ser C Life Sci, 2006, 49(1): 1-11.

[5]

Deans RM, Farquhar GD, Busch FA. Estimating stomatal and biochemical limitations during photosynthetic induction. Plant Cell Environ, 2019, 42(12): 3227-3240.

[6]

Devireddy AR, Zandalinas SI, Gómez-Cadenas A, Blumwald E, Mittler R. Coordinating the overall stomatal response of plants: rapid leaf-to-leaf communication during light stress. Sci Signal, 2018 11 518 eaam9514

[7]

Fernández-Marín B, Atherton J, Olascoaga B, Kolari P, Porcar-Castell A, García-Plazaola JI. When the sun never sets: daily changes in pigment composition in three subarctic woody plants during the summer solstice. Trees, 2018, 32(2): 615-630.

[8]

Foyer CH, Lopez-Delgado H, Dat JF, Scott IM. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant, 1997, 100(2): 241-254.

[9]

Gaupels F, Sarioglu H, Beckmann M, Hause B, Spannagl M, Draper J, Lindermayr C, Durner J. Deciphering systemic wound responses of the pumpkin extrafascicular phloem by metabolomics and stable isotope-coded protein labeling. Plant Physiol, 2012, 160(4): 2285-2299.

[10]

Guo ZX, Wang F, Xiang X, Ahammed GJ, Wang MM, Onac E, Zhou J, Xia XJ, Shi K, Yin X, Chen KS, Yu JQ, Foyer CH, Zhou YH. Systemic induction of photosynthesis via illumination of the shoot apex is mediated by phytochrome B, auxin and hydrogen peroxide in tomato. Plant Physiol, 2016, 172(2): 1259-1272.

[11]

Heil M, Ton J. Long-distance signalling in plant defence. Trends Plant Sci, 2008, 13(6): 264-272.

[12]

Hou F, Jin LQ, Zhang ZS, Gao HY. Systemic signalling in photosynthetic induction of Rumex K-1 (Rumex patientia × Rumex tianschaious) leaves. Plant Cell Environ, 2015, 38(4): 685-692.

[13]

Hung KT, Kao CH. Hydrogen peroxide is necessary for abscisic acid-induced senescence of rice leaves. J Plant Physiol, 2004, 161(12): 1347-1357.

[14]

Iio A, Fukasawa H, Nose Y, Naramoto M, Mizunaga H, Kakubari Y. Within-branch heterogeneity of the light environment and leaf temperature in a Fagus crenata crown and its significance for photosynthesis calculations. Trees, 2009, 23(5): 1053-1064.

[15]

Jiang YP, Cheng F, Zhou YH, Xia XJ, Mao WH, Shi K, Chen Z, Yu JQ. Cellular glutathione redox homeostasis plays an important role in the brassinosteroid-induced increase in CO2 assimilation in Cucumis sativus. New Phytol, 2012, 194(4): 932-943.

[16]

Kaiser E, Morales A, Harbinson J. Fluctuating light takes crop photosynthesis on a rollercoaster ride. Plant Physiol, 2018, 176(2): 977-989.

[17]

Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science, 1999, 284(5414): 654-657.

[18]

Koizumi H, Oshima Y. Light environment and carbon gain of understory herbs associated with sunflecks in a warm temperate deciduous forest in Japan. Ecol Res, 1993, 8(2): 135-142.

[19]

Lake JA, Quick WP, Beerling DJ, Woodward FI. Signals from mature to new leaves. Nature, 2001, 411(6834): 154-154.

[20]

Larkindale J, Huang B. Thermotolerance and antioxidant systems in Agrostis stolonifera: Involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol, 2004, 161(4): 405-413.

[21]

Leakey ADB, Scholes JD, Press MC. Physiological and ecological significance of sunflecks for dipterocarp seedlings. J Exp Bot, 2005, 56(411): 469-482.

[22]

Liu XJ, Xu N, Wu YN, Li JB, Zhang HX, Zhang HH. Photosynthesis, chilling acclimation and the response of antioxidant enzymes to chilling stress in mulberry seedlings. J For Res, 2019, 30(6): 2021-2029.

[23]

Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T. Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato–root-knot nematode interactions. New Phytol, 2006, 170(3): 501-512.

[24]

Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal, 2009, 2(84): ra45-ra45.

[25]

Morris H, Plavcová L, Gorai M, Klepsch MM, Kotowska M, Schenk HJ, Jansen S. Vessel-associated cells in angiosperm xylem: highly specialized living cells at the symplast–apoplast boundary. Am J Bot, 2018, 105(2): 151-160.

[26]

Naumburg E, Ellsworth DS. Photosynthetic sunfleck utilization potential of understory saplings growing under elevated CO2 in FACE. Oecologia, 2000, 122(2): 163-174.

[27]

Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT. Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot, 2002, 53(372): 1237-1247.

[28]

Pearcy RW. Sunflecks and photosynthesis in plant canopies. Ann Rev Plant Physiol, 1990, 41(1): 421-453.

[29]

Pearcy RW. Caldwell MM, Pearcy RW. Photosynthetic utilization of sunflecks: a temporally patchy resource on a time scale of seconds to minutes. Exploitation of environmental heterogeneity by plants: ecophysiological processes above- and belowground, 1994, San Diego: Academic Press 175 208

[30]

Pearcy RW, Gross LJ, He D. An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes. Plant Cell Environ, 1997, 20(4): 411-424.

[31]

Shah J. Plants under attack: systemic signals in defence. Curr Opin Plant Biol, 2009, 12(4): 459-464.

[32]

Strand DD, Livingston AK, Satoh-Cruz M, Froehlich JE, Maurino VG, Kramer DM. Activation of cyclic electron flow by hydrogen peroxide in vivo. Proc Natl Acad Sci USA, 2015, 112(17): 5539-5544.

[33]

Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF, Shuman JL, Luo XZ, Shah J, Schlauch K. Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell, 2013, 25(9): 3553-3569.

[34]

Szechyńska-Hebda M, Kruk J, Górecka M, Karpińska B, Karpiński S. Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis. Plant Cell, 2010, 22(7): 2201-2218.

[35]

Thomas PW, Woodward FI, Quick WP. Systemic irradiance signalling in tobacco. New Phytol, 2004, 161(1): 193-198.

[36]

Tomimatsu H, Tang YH. Elevated CO2 differentially affects photosynthetic induction response in two Populus species with different stomatal behavior. Oecologia, 2012, 169(4): 869-878.

[37]

Urban O, Košvancová M, Marek MV, Lichtenthaler HK. Induction of photosynthesis and importance of limitations during the induction phase in sun and shade leaves of five ecologically contrasting tree species from the temperate zone. Tree Physiol, 2007, 27(8): 1207-1215.

[38]

Valladares F, Allen MT, Pearcy RW. Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occuring along a light gradient. Oecologia, 1997, 111(4): 505-514.

[39]

Vialet-Chabrand S, Matthews JSA, Simkin AJ, Raines CA, Lawson T. Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiol, 2017, 173(4): 2163-2179.

[40]

Yano S, Terashima I. Separate localization of light signal perception for sun or shade type chloroplast and palisade tissue differentiation in Chenopodium album. Plant Cell Physiol, 2001, 42(12): 1303-1310.

[41]

Zhang ZS, Li YT, Gao HY, Yang C, Meng QW. Characterization of photosynthetic gas exchange in leaves under simulated adaxial and abaxial surfaces alternant irradiation. Sci Rep, 2016, 6: 26963.

[42]

Zhang ZS, Yang C, Gao HY, Zhang LT, Fan XL, Liu MJ. The higher sensitivity of PSI to ROS results in lower chilling-light tolerance of photosystems in young leaves of cucumber. J Photochem Photobiol B, 2014, 137: 127-134.

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