In Vivo Two-photon FLIM Resolves Photosynthetic Properties of Maize Bundle Sheath Cells

Overview

Journal Photosynth Res

Publisher Springer

Date 2025 Jan 21

PMID 39836265

Authors

Zhufeng Chen

Jing Li

Bai-Chen Wang

Lijin Tian

Affiliations

Soon will be listed here.

Abstract

Maize (Zea mays L.) performs highly efficient C photosynthesis by dividing photosynthetic metabolism between mesophyll and bundle sheath cells. In vivo physiological measurements are indispensable for C photosynthesis research as photosynthetic activities are easily interrupted by leaf section or cell isolation. Yet, direct in vivo observation regarding bundle sheath cells in the delicate anatomy of the C leaf is still challenging. In the current work, we used two-photon fluorescence-lifetime imaging microscopy (two-photon-FLIM) to access the photosynthetic properties of bundle sheath cells on intact maize leaves. The results provide spectroscopic evidence for the diminished total PSII activity in bundle sheath cells at its physiological level and show that the single PSIIs could undergo charge separation as usual. We also report an acetic acid-induced chlorophyll fluorescence quenching on intact maize leaves, which might be a physiological state related to the nonphotochemical quenching mechanism.

References

Bellasio C, Griffiths H . The operation of two decarboxylases, transamination, and partitioning of C4 metabolic processes between mesophyll and bundle sheath cells allows light capture to be balanced for the maize C4 pathway. Plant Physiol. 2013; 164(1):466-80. PMC: 3875822. DOI: 10.1104/pp.113.228221. View

Bhatti A, Kirilovsky D, van Amerongen H, Wientjes E . State transitions and photosystems spatially resolved in individual cells of the cyanobacterium Synechococcus elongatus. Plant Physiol. 2021; 186(1):569-580. PMC: 8154081. DOI: 10.1093/plphys/kiab063. View

Chukhutsina V, Bersanini L, Aro E, van Amerongen H . Cyanobacterial flv4-2 Operon-Encoded Proteins Optimize Light Harvesting and Charge Separation in Photosystem II. Mol Plant. 2015; 8(5):747-61. DOI: 10.1016/j.molp.2014.12.016. View

Chukhutsina V, Holzwarth A, Croce R . Time-resolved fluorescence measurements on leaves: principles and recent developments. Photosynth Res. 2018; 140(3):355-369. PMC: 6509100. DOI: 10.1007/s11120-018-0607-8. View

Chukhutsina V, Liu X, Xu P, Croce R . Light-harvesting complex II is an antenna of photosystem I in dark-adapted plants. Nat Plants. 2020; 6(7):860-868. DOI: 10.1038/s41477-020-0693-4. View

Eckardt N, Bock R, Croce R, Lagarias J, Merchant S, Redding K . Focus on photosynthesis. Plant Cell. 2024; 36(10):3895-3896. PMC: 11448878. DOI: 10.1093/plcell/koae204. View

Digman M, Caiolfa V, Zamai M, Gratton E . The phasor approach to fluorescence lifetime imaging analysis. Biophys J. 2007; 94(2):L14-6. PMC: 2157251. DOI: 10.1529/biophysj.107.120154. View

Ermakova M, Woodford R, Fitzpatrick D, Nix S, Zwahlen S, Farquhar G . Chloroplast NADH dehydrogenase-like complex-mediated cyclic electron flow is the main electron transport route in C bundle sheath cells. New Phytol. 2024; 243(6):2187-2200. DOI: 10.1111/nph.19982. View

Farooq S, Chmeliov J, Wientjes E, Koehorst R, Bader A, Valkunas L . Dynamic feedback of the photosystem II reaction centre on photoprotection in plants. Nat Plants. 2018; 4(4):225-231. DOI: 10.1038/s41477-018-0127-8. View

10.

Friso G, Majeran W, Huang M, Sun Q, van Wijk K . Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol. 2010; 152(3):1219-50. PMC: 2832236. DOI: 10.1104/pp.109.152694. View

11.

Hernandez-Prieto M, Foster C, Watson-Lazowski A, Ghannoum O, Chen M . Comparative analysis of thylakoid protein complexes in the mesophyll and bundle sheath cells from C , C and C -C Paniceae grasses. Physiol Plant. 2019; 166(1):134-147. DOI: 10.1111/ppl.12956. View

12.

Iermak I, Vink J, Bader A, Wientjes E, van Amerongen H . Visualizing heterogeneity of photosynthetic properties of plant leaves with two-photon fluorescence lifetime imaging microscopy. Biochim Biophys Acta. 2016; 1857(9):1473-1478. DOI: 10.1016/j.bbabio.2016.05.005. View

13.

Ishikawa N, Takabayashi A, Noguchi K, Tazoe Y, Yamamoto H, von Caemmerer S . NDH-Mediated Cyclic Electron Flow Around Photosystem I is Crucial for C4 Photosynthesis. Plant Cell Physiol. 2016; 57(10):2020-2028. DOI: 10.1093/pcp/pcw127. View

14.

Johnson M, Ruban A . Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J. 2009; 61(2):283-9. DOI: 10.1111/j.1365-313X.2009.04051.x. View

15.

Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta S . The developmental dynamics of the maize leaf transcriptome. Nat Genet. 2010; 42(12):1060-7. DOI: 10.1038/ng.703. View

16.

Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E . Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell. 2010; 22(11):3509-42. PMC: 3015116. DOI: 10.1105/tpc.110.079764. View

17.

Ogawa T, Kobayashi K, Taniguchi Y, Shikanai T, Nakamura N, Yokota A . Two cyclic electron flows around photosystem I differentially participate in C4 photosynthesis. Plant Physiol. 2023; 191(4):2288-2300. PMC: 10069883. DOI: 10.1093/plphys/kiad032. View

18.

Ouyang W, Wientjes E, van der Putten P, Caracciolo L, Zhao R, Agho C . Roles for leakiness and O evolution in explaining lower-than-theoretical quantum yields of photosynthesis in the PEP-CK subtype of C plants. New Phytol. 2024; 242(2):431-443. DOI: 10.1111/nph.19614. View

19.

Peterson R, Schultes N, McHale N, Zelitch I . Evidence for a Role for NAD(P)H Dehydrogenase in Concentration of CO2 in the Bundle Sheath Cell of Zea mays. Plant Physiol. 2016; 171(1):125-38. PMC: 4854706. DOI: 10.1104/pp.16.00120. View

20.

Pick T, Brautigam A, Schluter U, Denton A, Colmsee C, Scholz U . Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. Plant Cell. 2011; 23(12):4208-20. PMC: 3269860. DOI: 10.1105/tpc.111.090324. View