Journal of Plant Physiology 240 (2019) 153002

Contents lists available at ScienceDirect

Journal of Plant Physiology

journal homepage: www.elsevier.com/locate/jplph

Comparing two measures of leaf photorespiration rate across a wide range of T

light intensities
Zi-Piao Yea,1, Yu-Guo Liub,1, Hua-Jing Kangc, Hong-Lang Duand, Xian-Mao Chene, ,
⁎

Shuang-Xi Zhouf,
⁎

a
Maths and Physics College, Jinggangshan University, Ji’an 343009, Jiangxi, China
b
Institute of Desertification Studies, Chinese Academy of Forestry, Beijing 100091, China
c
Wenzhou Vocational College of Science and Technology, Wenzhou 325006, Zhejiang, China
d
Jiangxi Provincial Key Laboratory for Restoration of Degraded Ecosystems & Watershed Ecohydrology, Nanchang Institute of Technology, Nanchang 330099, China
e
Soil Fertilizer and Environmental Resources Institute, Jiangxi Academy of Agricultural Sciences, Nanchang 330200, Jiangxi, China
f
The New Zealand Institute for Plant and Food Research Limited, Hawke’s Bay 4130, New Zealand

ARTICLE INFO ABSTRACT

Keywords: Suppression of photorespiration by low O2 concentrations (Method 1) and simultaneous measurements of gas
Electron flow exchange and chlorophyll fluorescence (Method 2) are often used to estimate leaf photorespiration rate (Rp) of
Light response C3 plants. However, it is largely unknown whether Method 1 and Method 2 can be used equivalently in esti-
Photoprotection mating Rp. Using a field experiment on two wheat cultivars (T. aestivum JM22 and T. aestivum Z39-118) whose
Photorespiration
leaf gas exchange and chlorophyll fluorescence at low and normal O2 concentrations (2% versus 21% O2) were
Photosynthesis
Saturation light intensity
simultaneously measured across a wide range of light intensities (I), this study assessed the impacts of the two
measures on Rp and its response under changing irradiance conditions. All the above quantities increased with
the increasing I until reaching the cultivar-specific maximum values and the corresponding saturation light
intensities. However, there were significant differences between Rp estimated by Method 1 and Method 2 at the I
range from 150 to 2000 μmol m−2 s−1 for T. aestivum JM22 and from 150 to 1000 μmol m−2 s−1 for T. aestivum
Z39-118. These findings demonstrated that the two methods cannot be used equivalently under changing ir-
radiance conditions.

1. Introduction
Photorespiration is a process accompanying and competing with
photosynthesis in C3 plants, in which O2 competes with CO2 for the
active site of ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase
(Rubisco) and Rubisco oxygenates but does not carboxylate RuBP.
Besides consuming considerable energy, the photorespiratory pathway
can cause a loss of between 20% and 30% of carbon fixed in photo-
synthesis of C3 plants (Sharkey, 1988; Bauwe et al., 2010; Raines, 2011;
Bräutigam and Gowik, 2016). The rate of photorespiration in leaves
(Rp) has been a prime research target for quantifying CO2 fluxes at
different scales (Hanson et al., 2016) and improving crop productivity
in the face of a growing global population and climate change chal-
lenges (Bauwe et al., 2010; Raines, 2011; Walker et al., 2016). Although
Rp has been widely reported in both fundamental and applied research,
studies evaluating different measures of Rp are limited (Sharkey, 1988;

⁎
Corresponding authors.
E-mail addresses: chenxmtfs@126.com (X.-M. Chen), shuangxi.zhou@plantandfood.co.nz (S.-X. Zhou).
1
These authors contributed equally to this work.

https://doi.org/10.1016/j.jplph.2019.153002
Received 1 November 2018; Received in revised form 17 June 2019; Accepted 17 June 2019
Available online 21 June 2019
0176-1617/ © 2019 Elsevier GmbH. All rights reserved.
Z.-P. Ye, et al.
Fig. 1. Light-response curves of photosynthesis for two wheat cultivars at both 2% and 21% O2 concentration. Values are the means ± standard errors (n = 4–5).
Busch, 2013).
Two measures of Rp have been widely used in the past two decades,
in particular: (1) suppression of photorespiration by low O2 con-
centrations (hereafter, Method 1) (e.g. Björkman, 1966; Forrester et al.,
1966; Laing et al., 1974; Andersen et al., 1985; Sharkey, 1985; Sage and
Sharkey, 1987; Long and Bernacchi, 2003; Aliyev, 2012; Gu et al.,
2012; Ellsworth et al., 2015; Buckley et al., 2017; Gauthier et al., 2018)
and (2) simultaneous measurements of gas exchange and chlorophyll
fluorescence (hereafter, Method 2) (e.g. Long and Bernacchi, 2003; Fila
et al., 2006; Bagard et al., 2008; Bai et al., 2017; Lima Neto et al.,
2017).
In Method 1, when photosynthesis reaches the steady-state level,
the air with a low content of oxygen (e.g. 2% O2) is blown into the
chamber and the leaf gas exchange is measured. The value of Rp is
determined as the difference between the photosynthetic values under
low (i.e. 2% O2) and normal oxygen (i.e. 21% O2) conditions. In Method
2, leaf gas exchange and chlorophyll fluorescence are simultaneously
measured to obtain the total electron flow (JT), net photosynthetic rate
(An), and CO2 released through mitochondrial respiration or day re-
spiration rate (Rday). The value of Rp is directly calculated as Rp = [JT –
4(An + Rday)]/12.
It has not been tested whether there is significant difference be-
tween Rp estimated by the Method 1 and Method 2 under changing
irradiance conditions. In this study, we aimed to assess potential im-
pacts of two different estimation methods on Rp and the response of Rp
under changing irradiance conditions, by simultaneously measuring the
leaf gas exchange and chlorophyll fluorescence of two field-grown
wheat cultivars at low O2 concentrations (2% O2) and normal O2 con-
centrations (21% O2) across a wide range of light intensities.
2. Materials and methods
2.1. Experimental site and plant materials
The experiments were conducted at the Yucheng Comprehensive
2
Journal of Plant Physiology 240 (2019) 153002
Experiment Station of the Chinese Academy of Science (36°50′N,
116°34′E, 20.3 m), which is located along the lower reaches of the
Yellow River. The experimental station has a semi-arid climate, with an
annual mean temperature of 13.4 °C and a total annual mean pre-
cipitation of 567 mm. About 70% of annual precipitation occurs be-
tween June and September (based on historical weather data of
1985–2009). The soil is classified as a calcaric fluvisol according to the
FAO-UNESCO system, and the surface soil texture is silt loam
(sand = 12%, silt = 66%, clay = 22%) according to the USDA classi-
fication system, and has a pH of 8.6 (Hou et al., 2012).
Winter wheat (T. aestivum JM22 and Z39-118) was planted in field
on October 4th, 2011. During the growing seasons, maximum light in-
tensity reached ˜2000 μmol m−2 s−1 on sunny days. The measurements
were performed from 2–3rd May for T. aestivum JM22, 15–26th May for
T. aestivum Z39-118 in 2012.
2.2. Measurements of CO2 gas exchange and chlorophyll fluorescence
Following the methods described by Yoshimura (2001), Parys et al.
(2004), Gu et al. (2012), Kangasjärvi et al. (2012), and Gauthier et al.
(2018), the net photosynthetic rate (An), total photosynthetic electron
flow (JT), intercellular CO2 concentration (Ci), and stomatal con-
ductance (gs) were monitored using a portable LI-6400-40 photo-
synthesis system (Li-Cor, Lincoln, NE, USA) at 2% and 21% O2, re-
spectively. All measurements were conducted on the same mature and
fully expanded sunlit leaves in different monitoring events. The relative
humidity in the cuvette was maintained at 60%, and leaf temperature
was maintained throughout the measurement period at 35.0 °C and
30.0 °C for JM22 and Z39-118, respectively. Each leaf was placed in the
cuvette for 60 min to achieve a steady state prior to the gas exchange
measurements. Rp was determined by the difference between the pho-
tosynthetic values in low (e.g. 2% O2) and normal oxygen (e.g. 21% O2)
content of the air (Method 1).
Light-response curves of photosynthesis (An–I curves) and total
electron transport rate (JT–I curves) were generated by applying
Z.-P. Ye, et al. Journal of Plant Physiology 240 (2019) 153002

Fitted (Model 1) and measured values (Obs.) of parameters defining the light-response curve of photosynthesis for two wheat cultivar. The parameters are: initial slope of the An–I curve (α), the maximum net
photosynthetic rate (Anmax) and the corresponding saturation irradiance (Isat) and dark respiration rate (Rd). Values are the mean ± standard errors (n = 4–5). The different the letters denote statistically significant different light intensities in a descending order of 2000, 1800, 1600,

40.50 ± 0.46a

2.98 ± 0.26a
1400, 1200, 1000, 800, 600, 400, 200, 150, 100, 80, 50, and
0 μmol m−2 s−1, while ambient CO2 concentration of the cuvette (Ca)

> 2000
was kept constant at 380 μmol mol−1. For each I level, CO2 assimilation

Obs.
was monitored and data-logging was made after the steady state was

–
reached.
The total electron transport rate (JT) was calculated as JT = ΦPSII × I

2199.95 ± 53.46
0.098 ± 0.002
× 0.5 × 0.84, where I is the light intensity, 0.5 was used as the fraction
41.53 ± 0.58a

3.57 ± 0.18a
of excitation energy distributed to PSII (Ehleringer and Pearcy, 1983;
Krall and Edwards, 1992; Lima Neto et al., 2017), 0.84 was used as the
Model 1

0.9991
2% O2

fraction of incoming light absorbed by leaves (Major and Dunton, 2002;

Lima Neto et al., 2017), and ΦPSII is the effective quantum yield of PSII
(Genty et al., 1989; Krall and Edwards, 1992). When the other alter-
native electron sinks are ignored or kept constant (Long and Bernacchi,
1840.00 ± 40.00a

2003), the electron flow for RuBP carboxylation (JC) was calculated
30.12 ± 1.28a

2.98 ± 0.26a

following Valentini et al. (1995) as follows:

1
difference (p ≤ 0.05) between the values fitted by Model 1 and measured values (Obs.) for each parameter within each O2 concentration within each cultivar.

JC = [JT + 8(An + Rday )]

(1)
Obs.

3
–

The electron flow for RuBP oxygenation (Jo) was calculated as

follows:
T. aestivum Z39-118

1963.62 ± 77.26a

2
0.075 ± 0.002
29.71 ± 1.29a

JO = [JT 4(An + R day )]

3.19 ± 0.24a

3 (2)
Model 1
21% O2

The photorespiratory rate (Rp) was calculated following Long and

0.9985

Bernacchi, 2003Long and Bernacchi(2003) (Method 2) as follows:

Rp = [JT 4(An + Rday )] 12 (3)
These calculations required knowledge of Rday, which is usually
a
1960.00 ± 40.00

estimated by the respiration rate measured in the dark, Rd. This re-
44.56 ± 1.62a

3.30 ± 0.34a

presents a simplification, since it has been well established that mi-

tochondrial respiration is partly inhibited in the light (Brooks and
Farquhar, 1985; Atkin et al., 2000; Gauthier et al., 2018). According to
Obs.

Fila et al. (2006), Rday = 0.5 Rd.

An–I curves and JT–I curves were fitted using the same non-
asymptotic model developed by Ye (2007) and Ye et al. (2013) (here-
2012.37 ± 92.62a

after, Ye model) as follows:

0.096 ± 0.003
44.14 ± 1.59a

3.92 ± 0.30a

1 pI
Model 1

An = I Rd,
0.9990

p
2% O2

1+ pI (4)

1 eI
J= e I,
1+ eI (5)
1880.00 ± 80.00a

where αp is the initial slope of light-response curve of photosynthesis; βp

31.07 ± 2.62a

3.54 ± 0.39a

and γp are termed as photoinhibition coefficient and saturation coeffi-

cient, respectively; Rd is the dark respiratory rate, which can be ob-
tained at I =0 μmol m−2 s−1; J is the electron transport rate and I is the
Obs.

light intensity; αe is the initial slope of J–I curve; βe and γe are photo-
inhibition and saturation coefficients, respectively.
1941.07 ± 207.66a
T. aestivum JM22

2.3. Statistical analysis

0.068 ± 0.001
30.87 ± 2.57a

3.47 ± 0.40a

Data are expressed as the means ± standard error (SE). We used

Model 1
21% O2

0.9991

One-Way ANOVA to examine differences between Rp estimated by two

Coefficient of determination, R2
Anmax (μmol m−2 s-1)
)

Isat (μmol m s )
Rd (μmol m−2 s-1)
−1

−2 -1
αp (μmol μmol
Table 1

3
Z.-P. Ye, et al.
Fig. 2. Light-response curves of total photosynthetic electron flow for two wheat cultivars at both 2% and 21% O2 concentration. Values are the means ± standard
errors (n = 4–5).
introduced methods. Those differences were considered significant at p
≤ 0.05. Goodness of fit of the mathematical model to experimental
observations was assessed using the coefficient of determination (R2).
R2 = 1 – SSE/SST, where SST is the total sum of squares and the SSE is
the error sum of squares. All statistical tests were performed using the
statistical package SPSS 18.5 statistical software (SPSS, Chicago, IL).
3. Results
3.1. Light-response curves of An
The increase of I led to an immediate and rapid increase of An for
the two wheat cultivars until reaching the cultivar-specific An (Anmax) at
the corresponding saturation light intensity (Isat) (Fig. 1; Table 1). Anmax
at 2% O2 concentration was higher than at 21% O2 concentration for
the two wheat cultivars (not significant), whose photorespiration at low
O2 concentration was suppressed (Table 1). The Ye model was able to
characterize the An–I response curves for two wheat cultivars at both
2% and 21% O2 concentration levels (Fig. 1), and the values of Anmax
and other photosynthetic parameters calculated by the Ye model were
in close agreement with the measured values for the two wheat culti-
vars at 2% and 21% O2 (Table 1).
3.2. Light-response curves of JT
The increase of I led to an immediate and rapid increase of JT for the
two wheat cultivars until reaching the cultivar-specific maximum JT (JT-
max) at the corresponding saturation light intensity (PARsat) (Fig. 2;
Table 2). JT-max at 2% O2 concentration was lower than at 21% O2
concentration for the two wheat cultivars (not significant). The Ye
4
Journal of Plant Physiology 240 (2019) 153002
model was able to characterize the JT–I response curves for two wheat
cultivars both at 2% and 21% O2 (Fig. 2; Table 2), and the values of JT-
max calculated by the Ye model were in close agreement with the
measured values for the two wheat cultivars at 2% and 21% O2
(Table 2).
3.3. Light-response curves of Rp
Within the low range of I, Rp estimated by Method 1 increased faster
than Rp calculated by Eq. (3) (Method 2) with the increase of I (Fig. 3).
The maximum Rp (Rp-max) and the corresponding saturation irradiance
(Ip-sat) measured by Method 1 were higher than those calculated by
Method 2 (Table 3). The significant differences between Rp calculated
by the two methods were observed at the range of I from 150 to
2000 μmol m−2 s−1 for T. aestivum JM22 (P < 0.05) (Table 3;
Fig. 3A), and from 150 to 1000 μmol m−2 s−1 (except 200 μmol m−2
s−1) for T. aestivum Z39-118 (P < 0.05) (Table 3; Fig. 3B).
4. Discussions
To the best of our knowledge, it is largely unknown whether Method
1 and Method 2 can be used equivalently in estimating Rp under
changing irradiance conditions. This study compared the two methods
in estimating leaf photorespiration rate across a wide range of light
intensities, and highlighted that Rp (and thus JO) estimated by Method 1
was significantly higher than that estimated by Method 2 at the I range
from 150 to 2000 μmol m−2 s−1 for T. aestivum JM22 (P < 0.05)
(Table 3; Fig. 3A), and from 150 to 1000 μmol m−2 s−1 for T. aestivum
Z39-118 (Table 3; Fig. 3B).
Method 1 assumes the photorespiration-led decrease in An was
Z.-P. Ye, et al. Journal of Plant Physiology 240 (2019) 153002

Fitted (Model 1) and measured values (Obs.) of parameters defining light-response curve of electron transport rate for two wheat cultivars. The parameters are: the initial slope of JT–I curve (αe), the maximum total
photosynthetic electron flow (JT-max) and the corresponding saturation irradiance (PARsat). Values are the mean ± standard errors (n = 4–5). The different letters denote statistically significant difference (p ≤ 0.05) exclusively derived from the changed O2 concentration (Sharkey, 1988;

1450.00 ± 95.73a
Busch, 2013), which ignores that the O2 sensitivity of CO2 exchange can

146.37 ± 4.02a
be affected by the biochemical process limiting An (Sharkey, 1985; Sage
and Sharkey, 1987; Busch, 2013). Meanwhile, by comparing the elec-
tron flow through photosystem II (PSII) to oxygenation (JO) versus the

Obs.
electron flow for RuBP carboxylation (JC), Method 2 assumes that other

–
alternative electron sinks are negligible (Valentini et al., 1995). Both
simplifications can cause uncertainties in estimating Rp (Busch, 2013).

1533.60 ± 80.98a
139.34 ± 2.74a As there was no benchmarking measure on the actual Rp under
0.327 ± 0.009

changing irradiance conditions, our study can conclude neither that

Method 1 overestimated Rp nor that Method 2 underestimated Rp for
Model 1

0.9976
2% O2

the two cultivars. Underestimation of Rp can lead to (1) overestimation

of plant productivity (Aliyev, 2012), (2) underestimation of JO (Long
and Bernacchi, 2003) and the role of photorespiration in plant photo-
protection (Kangasjärvi et al., 2012), and (3) overestimation of JC when
1900.00 ± 57.74a

other alternative electron sinks are ignored (e.g. Long and Bernacchi,
244.92 ± 6.39a

2003; Fila et al., 2006; Bai et al., 2017).

Our study also highlighted that the Ye model can (1) reproduce An–I
curves and JT–I curves extremely well and (2) accurately fit Anmax and
Obs.

JT-max and other quantitative traits defining the curves – for the two
–

wheat cultivars at both 2% O2 and 21% O2 concentration levels.

between the values fitted by Model 1 and measured values (Obs.) for each parameter within each O2 concentration level within each wheat cultivar.

Studying light responses of Rp and JO (Rp–I and JO–I curves, respec-

1988.47 ± 107.72a
T. aestivum Z39-118

tively) can also provide important insight on dynamics of photo-

244.72 ± 6.28a
0.321 ± 0.001

synthetic products and photosynthetic electron flow under changing

irradiance conditions. Future studies using a similar model-observation
Model 1
21% O2

0.9980

intercomparison approach to quantitatively characterize Rp responses

to changing environmental conditions would be very helpful for scaling
up leaf-level Rp and modeling environmental change consequences on
global plant productivity.
1400.00 ± 141.42a

We conclude that Method 1 and Method 2 cannot be used equiva-

158.08 ± 7.69a

lently when estimating Rp (and JO). The findings in this study remain to
be tested for other species and/or plant functional types which could
display different response patterns.
Obs.

Acknowledgements
1453.54 ± 53.59a

This study was supported by the National Key Research and

161.58 ± 5.62a
0.282 ± 0.012

Development Program of China (Grant No. 2016 YFD 03001008),

Jiangxi Special Fund for Agro-scientific Research in the Collaborative
Model 1

Innovation (Grant No. JXXTCX2015001-005), the National Natural

0.9972
2% O2

Science Foundation of China (Grant No. 31560069), the Key Science

and Technology Innovation Team Project of Wenzhou City (Grant No.
C20150008), the Program for Construction of the Advantage Science
1840.00 ± 74.83a

and Technology Innovation Group of Jiangxi Province (Grant No.

248.12 ± 8.39a

20142BCB24010), the National Natural Science Foundation of China

(Grant No. 31500583), and the Chinese Academy of Forestry
Obs.

–
1927.19 ± 77.69a
T. aestivum JM22

246.27 ± 7.63a
0.295 ± 0.012
Model 1
21% O2

0.9994
Coefficient of determination, R2
JT-max (μmol m−2 s−1)
PARsat (μmol mol )−1
−1
αe (μmol μmol )
Table 2

5
Z.-P. Ye, et al. Journal of Plant Physiology 240 (2019) 153002

Fig. 3. Light-response curves of leaf photorespiration rate for two wheat cultivars. Values are the means ± standard errors (n = 4–5).

Table 3
Rp-max and Ip-sat calculated by Method 1 and Method 2 from light-response curve of photorespiration rate for two wheat cultivars. Values are the means ± standard
errors (n = 4–5). The different letters denote statistically significant difference (p ≤ 0.05) between the values fitted by Method 1 and 2 within each cultivar.
T. aestivum JM22 T. aestivum Z39-118

Method 1 Method 2 Method 1 Method 2

−2 −1 a b a
Rp-max (μmol m s ) 13.09 ± 0.85 10.02 ± 0.69 11.82 ± 0.94 9.50 ± 0.63a
Ip-sat (μmol m−2 s−1) 1840.00 ± 116.62a 1760.00 ± 74.83a 1600.00 ± 81.65a 1600.00 ± 81.65a

Foundation (Grant No. IDS2019JY-1). Cell Environ. 38, 1142–1156.

References
Aliyev, J.A., 2012. Photosynthesis, photorespiration and productivity of wheat and soy-
bean genotypes. Physiol. Plant. 145, 369–383.
Andersen, I.H., Dons, C., Nilsen, S., Haugstad, M.K., 1985. Growth, photosynthesis and
photorespiration of Lernna gibba: response to variations in CO2 and O2 concentrations
and photon flux density. Photosynth. Res. 6, 87–96.
Atkin, O.K., Evans, J.R., Ball, M.C., Lambers, H., Pons, T.L., 2000. Leaf respiration of snow
gum in the light and dark: interactions between temperature and irradiance. Plant
Physiol. 122, 915–923.
Bagard, M., Le Thiec, D., Delacote, E., Hasenfrantz-Sauder, M.P., Banvoy, J., Gérard, J.,
Dizengremel, P., 2008. Ozone-induced changes in photosynthesis and photorespira-
tion of hybrid poplar in relation to the developmental stage of the leaves. Plant
Physiol. 134, 559–574.
Bai, J., Kang, T., Wu, H., Lu, B., Long, X., Luo, X., Zhang, Y., Zhou, Y., Gong, C., 2017.
Relative contribution of photorespiration and antioxidative mechanisms in Caragana
korshinskii under drought conditions across the Loess Plateau. Funct. Plant Biol. 44,
1112–1123.
Bauwe, H., Hagemann, M., Fernie, A.R., 2010. Photorespiration: players, partners and
origin. Trends Plant Sci. 15, 330–336.
Björkman, O., 1966. The effect of oxygen concentration on photosynthesis in higher
plants. Physiol. Plant. 19, 618–633.
Bräutigam, A., Gowik, U., 2016. Photorespiration connects C3 and C4 photosynthesis. J.
Exp. Bot. 67 (10), 2953–2962.
Brooks, A., Farquhar, G.D., 1985. Effect of temperature on the CO2/O2, specificity of
ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the
light. Planta 165, 397–406.
Buckley, T.N., Vice, H., Adams, M.A., 2017. The Kok effect in Vicia faba cannot be ex-
plained solely by changes in chloroplastic CO2 concentration. New Phytol. 216,
1064–1071.
Busch, F.A., 2013. Current methods for estimating the rate of photorespiration in leaves.
Plant Biol. 15, 648–655.
Ehleringer, J., Pearcy, R.W., 1983. Variation in quantum yield for CO2 uptake among C3
and C4 plants. Plant Physiol. 73, 555–559.
Ellsworth, D.S., Crous, K.Y., Lambers, H., Cooke, J., 2015. Phosphorus recycling in
photorespiration maintains high photosynthetic capacity in woody cultivars. Plant
Forrester, M.L., Krotkov, G., Nelson, C.D., 1966. Effect of oxygen on photosynthesis,
photorespiration and respiration in detached leaves. I. soybean. Plant Physiol. 41,
422–427.
Fila, G., Badeck, F., Meyer, S., Cerovic, Z., Ghashghaie, J., 2006. Relationships between
leaf conductance to CO2 diffusion and photosynthesis in micropropagated grapevine
plants, before and after ex vitro acclimatization. J. Exp. Bot. 57, 2687–2695.
Gauthier, P.P., Battle, M.O., Griffin, K.L., Bender, M.L., 2018. Measurement of gross
photosynthesis, respiration in the light, and mesophyll conductance using H218O
labeling. Plant Physiol. 177, 62–74.
Genty, B., Briantais, J.M., Baker, N.R., 1989. The relationship between the quantum yield
of photosynthetic electron transport and quenching of chlorophyll fluorescence.
Biochim. Biophys. Acta 990, 87–92.
Gu, J., Yin, X., Stomph, T.J., Wang, H., Struik, P.C., 2012. Physiological basis of genetic
variation in leaf photosynthesis among rice (Oryza sativa L.) introgression lines under
drought and well-watered conditions. J. Exp. Bot. 63, 5137–5153.
Hanson, D.T., Stutz, S.S., Boyer, J.S., 2016. Why small fluxes matter: the case and ap-
proaches for improving measurements of photosynthesis and (photo) respiration. J.
Exp. Bot. 67 (10), 3027–3039.
Hou, R.X., Ouyang, Z., Li, Y.S., Tyler, D.D., Li, F.D., Wilson, G.V., 2012. Effects of tillage
and residue management on soil organic carbon and total nitrogen in the North China
plain. Soil Sci. Soc. Am. J. 76, 230–240.
Kangasjärvi, S., Neukermans, J., Li, S., Aro, E.-M., Noctor, G., 2012. Photosynthesis,
photorespiration, and light signalling in defence responses. J. Exp. Bot. 63,
1619–1636.
Krall, J.P., Edwards, G.E., 1992. Relationship between photosystem II activity and CO2
fixation in leaves. Physiol. Plant. 86, 180–187.
Laing, W.A., Ogren, W., Hageman, R.H., 1974. Regulation of soybean net photosynthetic
CO2 fixation by the interaction of CO2, O2 and ribulose1, 5-diphosphate carboxvlasel.
Plant Physiol. 54, 678–685.
Lima Neto, M.C., Cerqueira, J.V.A., Cunha, J.R.D., Ribeiro, R.V., Silveira, J.A.G., 2017.
Cyclic electron flow, NPQ and photorespiration are crucial for the establishment of
young plants of Ricinus communis and Jatropha curcas exposed to drought. Plant Biol.
19, 650–659.
Long, S.P., Bernacchi, C.J., 2003. Gas exchange measurements, what can they tell us
about the underlying limitations to photosynthesis? Procedures and sources of error.
J. Exp. Bot. 54, 2393–2401.
Major, K.M., Dunton, K.H., 2002. Variations in light-harvesting characteristics of the
seagrass, Thalassia testudinum: evidence for photoacclimation. J. Exp. Mar. Biol. Ecol.

6
Z.-P. Ye, et al.
275, 173–189.
Parys, E., Romanowska, E., Siedlecka, M., 2004. Light-enhanced dark respiration in leaves
and mesophyll protoplasts of pea in relation to photorespiration, respiration and
some metabolites content. Acta Physiol. Plant. 26, 37–46.
Raines, C.A., 2011. Increasing photosynthetic carbon assimilation in C3 plants to improve
crop yield: current and future strategies. Plant Physiol. 155, 36–42.
Sage, R.F., Sharkey, T.D., 1987. The effect of temperature on the occurrence of O2 and
CO2 insensitive photosynthesis in field-grown plants. Plant Physiol. 84, 658–664.
Sharkey, T.D., 1985. O2-insensitive photosynthesis in C3 plants – its occurrence and a
possible explanation. Plant Physiol. 78, 71–75.
Sharkey, T.D., 1988. Estimating the rate of photorespiration in leaves. Physiol. Plant. 73,
147–152.
Valentini, R., Epron, D., Angelis, P.D., Matteucci, G., Dreyer, E., 1995. In situ estimation of
net CO2 assimilation, photosynthetic electron flow and photorespiration of Turkey
Journal of Plant Physiology 240 (2019) 153002
oak (Q. cerris L.) leaves: diurnal cycles under different water supply. Plant Cell
Environ. 18, 631–640.
Walker, B.J., VanLoocke, A., Bernacchi, C.J., Ort, D.R., 2016. The costs of photo-
respiration to food production now and in the future. Annu. Rev. Plant Biol. 67,
107–129.
Ye, Z.P., 2007. A new model for relationship between irradiance and the rate of photo-
synthesis in Oryza sativa. Photosynthetica 45, 637–640.
Ye, Z.P., Suggett, J.D., Robakowski, P., Kang, H.J., 2013. A mechanistic model for the
photosynthesis-light response based on the photosynthetic electron transport of PS II
in C3 and C4 cultivars. New Phytol. 152, 1251–1262.
Yoshimura, Y., Kubota, F., Hirao, K., 2001. Estimation of photorespiration rate by si-
multaneous measurements of CO2, gas exchange rate, and chlorophyll fluorescence
quenching in the C3 plant Vigna radiata (L.) wilczek and the C4 plant Amaranthus
mongostanus L. Photosynthetica 39, 377–382.