Badeck FW, Tcherkez G, Nogués S, Piel C, Ghashghaie J. 2005.
Post-photosynthetic fractionation of stable carbon isotopes between plant organs—a widespread phenomenon. Rapid Communications in Mass Spectrometry 19:1381–1391. doi:10.1002/
rcm.1912.
Bellasio C, Farquhar GD. 2019. A leaf-level biochemical model simulating the introduction of C2 and C4 photosynthesis in C3 rice:
gains, losses and metabolite fluxes. New Phytologist 223:150–166.
doi:10.1111/nph.15787.
Berveiller D, Damesin C. 2008. Carbon assimilation by tree stems: potential involvement of phosphoenolpyruvate carboxylase. Trees
22:149–157. doi:10.1007/s00468-007-0193-4.
Berveiller D, Kierzkowski D, Damesin C. 2007. Interspecific variability
of stem photosynthesis among tree species. Tree Physiology 27:53–
61. doi:10.1093/treephys/27.1.53.
Bianconi ME, Hackel J, Vorontsova MS, Alberti A, Arthan W, Burke
SV, Duvall MR, Kellogg EA, Lavergne S, McKain MR, et al. 2020.
Downloaded from https://academic.oup.com/aobpla/article/15/4/plad046/7218885 by Kyoto-u Kokoro user on 01 November 2023
In spring, the bamboo shoots emerge, and the developing bamboos enter a phase of active and very rapid growth. Because
the leaf of new-born bamboo had not yet developed, the main
sources of carbohydrates during the FGP were supplied by
mature bamboos and delivered through their belowground
system to the developing culms, which is consistent with a
slight 13C enrichment of the bulk organic matter of immature
bamboos. Although previous studies observed key enzymes
related to C4 carbon fixation, the results based on 13C pulse labelling showed limited CO2 uptake from the atmosphere and
hollow during the FGP. Limited anaplerotic dark fixation of
CO2 is more likely to occur than C4 photosynthetic C fixation.
10
Ghashghaie J, Badeck FW, Lanigan G, Nogués S, Tcherkez G, Deleens
E, Cornic G, Griffiths H. 2003. Carbon isotope fractionation
during dark respiration and photorespiration in C3 plants. Phytochemistry Reviews 2:145–161.
Gilbert A, Robins RJ, Remaud GS, Tcherkez GGB. 2012. Intramolecular 13C pattern in hexoses from autotrophic and heterotrophic C3
plant tissues. Proceedings of the National Academy of Sciences
of the United States of America 109:18204–18209. doi:10.1073/
pnas.1211149109.
Hanba YT, Kobayashi T, Enomoto T. 2010. Variations in the foliar δ13C
and C3/C4 species richness in the Japanese flora of Poaceae among
climates and habitat types under human activity. Ecological Research 25:213–224. doi:10.1007/s11284-009-0652-z.
Helle G, Schleser G. 2004. Beyond CO2 fixation by Rubisco—an interpretation of 13C/12C variations in tree rings from novel intraseasonal studies on broad-leaf trees. Plant, Cell & Environment
27:367–380. doi:10.1111/j.0016-8025.2003.01159.x.
Hibberd JM, Quick WP. 2002. Characteristics of C4 photosynthesis in
stems and petioles of C3 flowering plants. Nature 415:451–454.
doi:10.1038/415451a.
Höll W. 1974. Dark CO2 fixation by cell-free preparations of the wood
of Robinia pseudoacacia. Canadian Journal of Botany 52:727–734.
doi:10.1139/b74-094.
Kiyama S. 1905. About the gas inside the bamboo culms. Tokyo
Kagakai Kaishi 26:333–357. doi:10.1246/nikkashi1880.26.333.
Kodama N, Barnard RL, Salmon Y, Weston C, Ferrio JP, Holst J, Werner
RA, Saurer M, Rennenberg H, Buchmann N, et al. 2008. Temporal
dynamics of the carbon isotope composition in a Pinus sylvestris
stand: from newly assimilated organic carbon to respired carbon dioxide. Oecologia 156:737–750. doi:10.1007/s00442-008-1030-1.
Langenfeld-Heyser R. 1989. CO2 fixation in stem slices of Picea
abies (L.) Karst: microautoradiographic studies. Trees 3:24–32.
doi:10.1007/BF00202397.
Li X, Ye C, Fang D, Zeng Q, Cai Y, Du H, Mei T, Zhou G. 2022. Nonstructural carbohydrate and water dynamics of Moso bamboo
during its explosive growth period. Frontiers in Forests and Global
Change 5:938941. doi:10.3389/gc.2022.9389.
Lundgren MR, Christin PA, Escobar EG, Ripley BS, Besnard G, Long
CM, Hattersley PW, Ellis RP, Leegood RC, Osborne CP. 2016.
Evolutionary implications of C3–C4 intermediates in the grass
Alloteropsis semialata. Plant, Cell & Environment 39:1874–1885.
doi:10.1111/pce.12665.
Müller R, Baier M, Kaiser WM. 1991. Differential stimulation of
PEP-carboxylation in guard cells and mesophyll cells by ammonium and fusicoccin. Journal of Experimental Botany 42:215–220.
doi:10.1093/jxb/42.2.215.
Nalborczyk E. 1978. Dark carboxylation and its possible effect on the
values of δ13C in C3 plants. Acta Physiologiae Plantarum 1:53–58.
Porra RJ, Thompson WA, Kriedemann PE. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents:
verification of the concentration of chlorophyll standards by atomic
absorption spectroscopy. Biochimica et Biophysica Acta - Bioenergetics 975:384–394. doi:10.1016/S0005-2728(89)80347-0.
Qi H, Coplen TB, Geilmann H, Brand WA, Böhlke JK. 2003. Two new
organic reference materials for δ13C and δ15N measurements and a
new value for the δ13C of NBS 22 oil. Rapid Communications in
Mass Spectrometry 17:2483–2487. doi:10.1002/rcm.1219.
Qi H, Coplen TB, Mroczkowski SJ, Brand WA, Brandes L, Geilmann
H, Schimmelmann A. 2016. A new organic reference material,
l-glutamic acid, USGS41a for δ13C and δ15N measurements—a
replacement for USGS41. Rapid Communications in Mass Spectrometry 30:859–866. doi:10.1002/rcm.7510.
R Core Team. 2023. R: a language and environment for statistical computing, v.4.2.2. Vienna, Austria: R foundation for Statistical Computing. http://www.r-project.org
Reed AH, Henry RJ, Mason WB. 1971. Influence of statistical method
used on the resulting estimate of normal range. Clinical Chemistry
17:275–284. doi:10.1093/clinchem/17.4.275.
Downloaded from https://academic.oup.com/aobpla/article/15/4/plad046/7218885 by Kyoto-u Kokoro user on 01 November 2023
Continued adaptation of C4 photosynthesis after an initial burst of
changes in the Andropogoneae grasses. Systematic Biology 69:445–
461. doi:10.1093/sysbio/syz066.
Bowling DR, Pataki DE, Randerson JT. 2008. Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytologist 178:24–
40. doi:10.1111/j.1469-8137.2007.02342.x.
Cernusak LA, Marshall JD. 2000. Photosynthetic refixation in
branches of Western white pine. Functional Ecology 14:300–311.
doi:10.1046/j.1365-2435.2000.00436.x.
Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl
A, Barbour MM, Williams DG, Reich PB, Ellsworth DS, et al.
2009. Viewpoint: why are non-photosynthetic tissues generally 13C
enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. Functional Plant Biology 36:199–213.
doi:10.1071/FP08216.
Chang WJ, Chang MJ, Chang ST, Yeh TF. 2013. Chemical composition
and immunohistological variations of a growing bamboo shoot.
Journal of Wood Chemistry and Technology 33:144–155. doi:10.1
080/02773813.2013.769114.
Chen M, Guo L, Ramakrishnan M, Fei Z, Vinod KK, Ding Y, Jiao
C, Gao Z, Zha R, Wang C, et al. 2022. Rapid growth of Moso
bamboo (Phyllostachys edulis): cellular roadmaps, transcriptome
dynamics, and environmental factors. Plant Cell 34:3577–3610.
doi:10.1093/plcell/koac193.
Chen M, Ju Y, Ahmad Z, Yin Z, Ding Y, Que F, Yan J, Chu J, Wei Q.
2021. Multi-analysis of sheath senescence provides new insights
into bamboo shoot development at the fast growth stage. Tree
Physiology 41:491–507. doi:10.1093/treephys/tpaa140.
Coplen TB, Brand WA, Gehre M, Gröning M, Meijer HAJ, Toman B,
Verkouteren RM. 2006. New guidelines for δ13C measurements.
Analytical Chemistry 78:2439–2441. doi:10.1021/ac052027c.
Damesin C. 2003. Respiration and photosynthesis characteristics of
current-year stems of Fagus sylvatica: from the seasonal pattern to
an annual balance. New Phytologist 158:465–475.
Damesin C, Lelarge C. 2003. Carbon isotope composition of currentyear shoots from Fagus sylvatica in relation to growth, respiration and use of reserves. Plant, Cell & Environment 26:207–219.
doi:10.1046/j.1365-3040.2003.00951.x.
Deleens E, Garnier-Dardart J. 1977. Carbon isotope composition
of biochemical fractions isolated from leaves of Bryophyllum
daigremontianum berger, a plant with crassulacean acid metabolism: some physiological aspects related to CO2 dark fixation.
Planta 135:241–248. doi:10.1007/BF00384896.
Desalme D, Priault P, Gérant D, Dannoura M, Maillard P, Plain C, Epron D.
2017. Seasonal variations drive short-term dynamics and partitioning
of recently assimilated carbon in the foliage of adult beech and pine.
New Phytologist 213:140–153. doi:10.1111/nph.14124.
Gessler A, Keitel C, Kodama N, Weston C, Winters AJ, Keith H, Grice K,
Leuning R, Farquhar GD. 2007. δ13C of organic matter transported
from the leaves to the roots in Eucalyptus delegatensis: short-term
variations and relation to respired CO2. Functional Plant Biology
34:692–706. doi:10.1071/FP07064.
Gessler A, Ferrio JP, Hommel R, Treydte K, Werner RA, Monson RK.
2014. Stable isotopes in tree rings: towards a mechanistic understanding of isotope fractionation and mixing processes from the
leaves to the wood. Tree Physiology 34:796–818. doi:10.1093/
treephys/tpu040.
Gessler A, Tcherkez G, Karyanto O, Keitel C, Ferrio JP, Ghashghaie J,
Kreuzwieser J, Farquhar GD. 2009. On the metabolic origin of the
carbon isotope composition of CO2 evolved from darkened lightacclimated leaves in Ricinus communis. New Phytologist 181:374–
386. doi:10.1111/j.1469-8137.2008.02672.x.
Gessler A, Tcherkez G, Peuke AD, Ghashghaie J, Farquhar GD. 2008.
Experimental evidence for diel variations of the carbon isotope
composition in leaf, stem and phloem sap organic matter in Ricinus
communis. Plant, Cell and Environment 31:941–953.
Ghashghaie J, Badeck FW. 2014. Opposite carbon isotope discrimination during dark respiration in leaves versus roots—a review. New
Phytologist 201:751–769. doi:10.1111/nph.12563.
AoB PLANTS, 2023, Vol. 15, No. 4
Wang et al. ― Carbon supporting the fast growth of immature bamboo culms
analysis. Rapid Communications in Mass Spectrometry 15:1136–
1140. doi:10.1002/rcm.353.
Wang L, Li Q, Gao P, Wei S, Lu J, Gao Y, Zhang R. 2021. Activities of
key enzymes involved in photosynthesis and expression patterns of
corresponding genes during rapid growth of Phyllostachys edulis.
Journal of Zhejiang A&F University 38:84–92. doi:10.11833/j.
issn.2095-0756.20200277.
Wang S, Chen TH, Liu EU, Liu CP. 2020. Accessing the nursing behaviour of Moso bamboo (Phyllostachys edulis) on carbohydrates dynamics and photosystems. Scientific Reports 10:1015. doi:10.1038/
s41598-020-57643-1.
Wang X, Liu L, Zhang J, Wang Y, Wen G, Gao R, Gao Y, Zhang R.
2012. Changes of photosynthetic pigment and photosynthetic enzyme activity in stems of Phyllostachys pubescens during rapid
growth stage after shooting. Chinese Journal of Plant Ecology
36:456–462. doi:10.3724/SP.J.1258.2012.00456.
Wittmann C, Hans M, van Winden WA, Ras C, Heijnen JJ. 2005. Dynamics of intracellular metabolites of glycolysis and TCA cycle
during cell-cycle-related oscillation in Saccharomyces cerevisiae.
Biotechnology and Bioengineering 89:839–847. doi:10.1002/
bit.20408.
Yen TM. 2016. Culm height development, biomass accumulation
and carbon storage in an initial growth stage for a fast growing
Moso bamboo (Phyllostachy pubescens). Botanical Studies 57:10.
doi:10.1186/s40529-016-0126-x.
Yen TM, Lee JS. 2011. Comparing aboveground carbon sequestration
between Moso bamboo (Phyllostachys heterocycla) and China fir
(Cunninghamia lanceolata) forests based on the allometric model.
Forest Ecology and Management 261:995–1002. doi:10.1016/j.
foreco.2010.12.015.
Zachariah EJ, Sabulal B, Nair DNK, Johnson AJ, Kumar CSP. 2016.
Carbon dioxide emission from bamboo culms. Plant Biology
18:400–405. doi:10.1111/plb.12435.
Zhai W, Wang Y, Luan J, Liu S. 2022. Effects of nitrogen addition
on clonal integration between mother and daughter ramets of
Moso bamboo: a 13C-CO2 pulse labeling study Zhang W-H
(ed). Journal of Plant Ecology 15:756–770. doi:10.1093/jpe/
rtab115.
Zhang M, Chen S, Jiang H, Cao Q. 2020. The water transport profile
of Phyllostachys edulis during the explosive growth phase of
bamboo shoots. Global Ecology and Conservation 24:e01251.
doi:10.1016/j.gecco.2020.e01251.
Downloaded from https://academic.oup.com/aobpla/article/15/4/plad046/7218885 by Kyoto-u Kokoro user on 01 November 2023
Richter A, Wanek W, Werner RA, Ghashghaie J, Jäggi M, Gessler A,
Brugnoli E, Hettmann E, Göttlicher SG, Salmon Y, et al. 2009.
Preparation of starch and soluble sugars of plant material for the
analysis of carbon isotope composition: a comparison of methods.
Rapid Communications in Mass Spectrometry 23:2476–2488.
doi:10.1002/rcm.4088.
Rossmann A, Butzenlechner M, Schmidt HL. 1991. Evidence for a
nonstatistical carbon isotope distribution in natural glucose. Plant
Physiology 96:609–614. doi:10.1104/pp.96.2.609.
Shi J, Mao S, Wang L, Ye X, Wu J, Wang G, Chen F, Yang Q. 2021.
Clonal integration driven by source-sink relationships is constrained
by rhizome branching architecture in a running bamboo species
(Phyllostachys glauca): a 15N assessment in the field. Forest Ecology
and Management 481:118754. doi:10.1016/j.foreco.2020.118754.
Shi M, Zhang J, Sun J, Li Q, Lin X, Song X. 2022. Unequal nitrogen translocation pattern caused by clonal integration between
connected ramets ensures necessary nitrogen supply for young
Moso bamboo growth. Environmental and Experimental Botany
200:104900. doi:10.1016/j.envexpbot.2022.104900.
Smith RG, Gauthier DA, Dennis DT, Turpin DH. 1992. Malate- and
pyruvate-dependent fatty acid synthesis in leucoplasts from
developing castor endosperm. Plant Physiology 98:1233–1238.
doi:10.1104/pp.98.4.1233.
Song X, Peng C, Zhou G, Gu H, Li Q, Zhang C. 2016. Dynamic allocation and transfer of non-structural carbohydrates, a possible mechanism for the explosive growth of Moso bamboo (Phyllostachys
heterocycla). Scientific Reports 6:25908. doi:10.1038/srep25908.
Tcherkez G, Nogués S, Bleton J, Cornic G, Badeck F, Ghashghaie J.
2003. Metabolic origin of carbon isotope composition of leaf
dark-respired CO2 in French Bean. Plant Physiology 131:237–244.
doi:10.1104/pp.013078.
Uchida EM, Katayama A, Yasuda Y, Enoki T, Otsuki K, Koga S, Utsumi
Y. 2022. Age-related changes in culm respiration of Phyllostachys
pubescens culms with their anatomical and morphological traits.
Frontiers in Forests and Global Change 5:868732. doi:10.3389/
ffgc.2022.868732.
Vuorinen AH, Kaiser WM. 1997. Dark CO2 fixation by roots of willow and barley in media with a high level of inorganic carbon.
Journal of Plant Physiology 151:405–408. doi:10.1016/S01761617(97)80004-1.
Wanek W, Heintel S, Richter A. 2001. Preparation of starch and other
carbon fractions from higher plant leaves for stable carbon isotope
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