title: Systemic Induction of Photosynthesis via Illumination of the Shoot Apex Is Mediated Sequentially by Phytochrome B, Auxin and Hydrogen Peroxide in Tomato.
abstract: Systemic signaling of upper leaves promotes the induction of photosynthesis in lower leaves, allowing more efficient use of light flecks. However, the nature of the systemic signals has remained elusive. Here, we show that preillumination of the tomato (Solanum lycopersicum) shoot apex alone can accelerate photosynthetic induction in distal leaves and that this process is light quality dependent, where red light promotes and far-red light delays photosynthetic induction. Grafting the wild-type rootstock with a phytochome B (phyB) mutant scion compromised light-induced photosynthetic induction as well as auxin biosynthesis in the shoot apex, auxin signaling, and RESPIRATORY BURST OXIDASE HOMOLOG1 (RBOH1)-dependent hydrogen peroxide (H2O2) production in the systemic leaves. Light-induced systemic H2O2production in the leaves of the rootstock also was absent in plants grafted with an auxin-resistant diageotropica (dgt) mutant scion. Cyclic electron flow around photosystem I and associated ATP production were increased in the systemic leaves by exposure of the apex to red light. This enhancement was compromised in the systemic leaves of the wild-type rootstock with phyB and dgt mutant scions and also in RBOH1-RNA interference leaves with the wild type as scion. Silencing of ORANGE RIPENING, which encodes NAD(P)H dehydrogenase, compromised the systemic induction of photosynthesis. Taken together, these results demonstrate that exposure to red light triggers phyB-mediated auxin synthesis in the apex, leading to H2O2generation in systemic leaves. Enhanced H2O2levels in turn activate cyclic electron flow and ATP production, leading to a faster induction of photosynthetic CO2assimilation in the systemic leaves, allowing plants better adaptation to the changing light environment.
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Zhixin
authors.initials: Z
authors.lastname: Guo
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Feng
authors.identifier: 0000-0001-5351-1531
authors.initials: F
authors.lastname: Wang
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Xun
authors.identifier: 0000-0001-9943-9977
authors.initials: X
authors.lastname: Xiang
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Golam Jalal
authors.initials: GJ
authors.lastname: Ahammed
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Mengmeng
authors.initials: M
authors.lastname: Wang
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Eugen
authors.identifier: 0000-0001-7292-9802
authors.initials: E
authors.lastname: Onac
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Jie
authors.initials: J
authors.lastname: Zhou
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Xiaojian
authors.initials: X
authors.lastname: Xia
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Kai
authors.initials: K
authors.lastname: Shi
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Xueren
authors.initials: X
authors.lastname: Yin
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Kunsong
authors.initials: K
authors.lastname: Chen
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Jingquan
authors.initials: J
authors.lastname: Yu
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.).
authors.forename: Christine H
authors.identifier: 0000-0001-5989-6989
authors.initials: CH
authors.lastname: Foyer
authors.affiliation: Department of Horticulture, Zijingang Campus, Zhejiang University, Hangzhou 310058, People's Republic of China (Z.G., F.W., Xu.X., G.J.A., J.Z., Xi.X., K.S., X.Y., K.C., J.Y., Y.Z.);Philips Research Europe, High Tech Campus 34, 5656 AE Eindhoven, The Netherlands (M.W., E.O.);Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, People's Republic of China (K.C., J.Y., Y.Z.); andCentre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom (C.H.F.) yanhongzhou@zju.edu.cn.
authors.forename: Yanhong
authors.initials: Y
authors.lastname: Zhou
mesh_terms: D000255:Adenosine Triphosphate / Q000096:biosynthesis; D004579:Electron Transport / Q000235:genetics / Q000528:radiation effects; D018506:Gene Expression Regulation, Plant / Q000528:radiation effects; D006861:Hydrogen Peroxide / Q000378:metabolism*; D007210:Indoleacetic Acids / Q000378:metabolism*; D008027:Light; D018551:Solanum lycopersicum / Q000235:genetics / Q000378:metabolism / Q000528:radiation effects*; D009154:Mutation; D009252:NADPH Dehydrogenase / Q000235:genetics / Q000378:metabolism; D019255:NADPH Oxidases; D010788:Photosynthesis / Q000235:genetics / Q000528:radiation effects*; D051939:Phytochrome B / Q000235:genetics / Q000378:metabolism*; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism / Q000528:radiation effects; D010940:Plant Proteins; D018520:Plant Shoots / Q000235:genetics / Q000378:metabolism / Q000528:radiation effects*; D030821:Plants, Genetically Modified; D034622:RNA Interference; D020133:Reverse Transcriptase Polymerase Chain Reaction
chemical_list: D007210:Indoleacetic Acids; D010940:Plant Proteins; D051939:Phytochrome B; D000255:Adenosine Triphosphate; D006861:Hydrogen Peroxide; D019255:NADPH Oxidases; C000611454:respiratory burst oxidase 1, tomato; D009252:NADPH Dehydrogenase