Chen et al.

Botanical Studies (2024) 65:10 Botanical Studies

https://doi.org/10.1186/s40529-024-00416-0

ORIGINAL ARTICLE Open Access

Gas exchange and chlorophyll fluorescence

responses of Camellia sinensis grown under
various cultivations in different seasons
Chung-I Chen1†, Kuan-Hung Lin2†, Meng-Yuan Huang3, Chih-Kai Yang1, Yu-Hsiu Lin4, Mei-Li Hsueh4, Li-Hua Lee4,
Shiou-Ruei Lin5* and Ching-Wen Wang4*

Abstract
Sod culture (SC) and conventional agriculture (CA) represent two distinct field management approaches utilized
in the cultivation of tea plants in Taiwan. In this study, we employed gas exchange and chlorophyll fluorescence
techniques to assess the impact of SC and CA methods on the photosynthetic machinery of Camellia sinensis cv.
TTES No.12 (Jhinhsuan) in response to variable light intensities across different seasons. In spring, at photosynthetic
photon flux densities (PPFD) ranging from 800 to 2,000 μmol photon m-2 s-1, the net photosynthesis rate (Pn,
10.43 μmol CO2 m-2 s-1), stomatal conductance (Gs, 126.11 mmol H2O m-2 s-1), electron transport rate (ETR, 137.94),
and ΔF/Fm’ and Fv/Fm (50.37) values for plants grown using SC were comparatively higher than those cultivated
under CA. Conversely, the non-photochemical quenching (NPQ) values for SC-grown plants were relatively lower
(3.11) compared to those grown under CA at 800 to 2,000 PPFD in spring. Additionally, when tea plants were
exposed to PPFD levels below 1,500 μmol photon m− 2 s− 1, there was a concurrent increase in Pn, Gs, ETR, and
NPQ. These photosynthetic parameters are crucial for devising models that optimize cultivation practices across
varying seasons and specific tillage requirements, and for predicting photosynthetic and respiratory responses of
tea plants to seasonally or artificially altered light irradiances. The observed positive impacts of SC on maximum
photosynthetic rate (Amax), Fv/Fm, Gs, water-use efficiency (WUE), and ETR suggest that SC is advantageous for
enhancing the productivity of tea plants, thereby offering a more adaptable management model for tea gardens.
Keywords Chlorophyll fluorescence, Photosynthetic capacity, Tea plant, Sod culture

†
Chung-I Chen and Kuan-Hung Lin contributed equally to this work.
Introduction
Tea (Camellia sinensis L.) stands as the most widely
*Correspondence:
Shiou-Ruei Lin consumed natural non-alcoholic beverage worldwide,
[email protected] renowned for its rich content of polyphenolic compounds
Ching-Wen Wang and specialized metabolites (Zeng et al. 2019; Zhang et
[email protected]
1
Department of Forestry, National Pingtung University of Science and al. 2020), which are deemed beneficial for human health
Technology, Pingtung County 91201, Taiwan (Hayat et al. 2015). Representing a lucrative cash crop, the
2
Department of Horticulture and Biotechnology, Chinese Culture global tea harvest amounted to 5.81 million tons, valued
University, Taipei City 11114, Taiwan
3
Department of Life Sciences and Innovation and Development Center of at approximately US $50 billion in 2018 (International
Sustainable Agriculture, National Chung Hsing University, Tea Committee, ITC 2021). Specifically, in Taiwan, the
Taichung City 40227, Taiwan tea yield reached approximately 14,341 kg, corresponding
4
Taiwan Biodiversity Research Institute, Nantou County 552, Taiwan
5
Tea and Beverage Research Station, Taoyuan City 326, Taiwan to a value of about US $0.4 billion in 2022 (Agriculture

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Chen et al. Botanical Studies (2024) 65:10 Page 2 of 12

and Food Agency, COA, 2023). One particular cultivar, of CO2 (Rd), light quantum yield of CO2 (Qy), light com-
Camellia sinensis cv. TTES No.12 (Jhinhsuan), stands out pensation point (LCP), and maximum net assimilation
as a globally acclaimed Oolong tea variety. of CO2 (Amax). These variables are crucial indicators of
Conventional agriculture (CA) involves the use of plant growth and metabolism influenced by climatic fac-
various pesticides, including herbicides, fungicides, and tors, such as light intensity (Chen et al. 2021).
insecticides, in farming operations. This practice often In habitats with full sun exposure, leaves often absorb
results in pesticide residues in the soil, pollution of nat- more photons than they can utilize, leading to a reduc-
ural resources, a reduction in biodiversity, and adverse tion in the photochemical efficiency of PSII in plants due
impacts on food security (Ferdous et al., 2021; Riedo et to the excess absorbed energy. High irradiance may cause
al., 2021). On the other hand, sod culture (SC) is a form photoinhibition, characterized by a loss of PSII activ-
of conservation agriculture that promotes sustainable ity and a light-dependent reduction in the fundamental
development by enhancing soil organic matter content, quantum yield of photosynthesis. This requires the dis-
sequestering organic carbon, improving soil physico- sipation of excess excitation energy (Portela et al. 2019).
chemical properties, increasing soil water-holding capac- Non-photochemical quenching (NPQ) is crucial for pho-
ity, advancing microorganism growth and biodiversity, toprotection as it quenches excess energy and safely dis-
increasing crop quality, reducing disease and pest dam- sipates it as heat (Murchie and Niyogi 2010). A higher
age, and improving the garden microclimate (Wang et NPQ serves as a protective mechanism against photoin-
al. 2016; Zou et al. 2016; Bai et al. 2017; Lin et al., 2019). hibition and photo-oxidation damage (Feng et al. 2002).
However, there is a lack of information on the impact of Additionally, plants exposed to strong light often exhibit
CA and SC on the photosynthetic physiology of tea fields decreases or adjustments in their leaf photosynthetic pig-
across different seasons and under varying light intensi- ment contents, which is an important photo-protective
ties. Tea plants are extensively cultivated in many coun- mechanism (Souza et al. 2017).
tries, but they frequently encounter challenges related to In a previous study, we found that an increase in Pn
both high and low irradiance throughout their life cycle enhanced the positive effects of Amax, maximum quan-
and growth process. This variability in light intensity tum efficiency of PSII photochemistry (Fv/Fm), Gs, water
affects the geographical distribution of tea plants and sig- use efficiency (WUE), electron transport rate (ETR), and
nificantly limits tea yield and quality (Liu et al. 2017; Dai non-photochemical quenching (NPQ) in SC citrus dur-
et al. 2015; Kfoury et al. 2018; Wen et al. 2020; Zhang et ing spring (Chen et al. 2021). This indicates that elevated
al. 2014, 2018, 2020; Xiang et al. 2021). Therefore, under- Pn can benefit citrus production and increase resilience
standing the photosynthetic characteristics of tea plants to stress under SC in the central region of Taiwan, con-
and identifying effective techniques to improve their sidering future climate scenarios. It is essential to quan-
tolerance to high and low light intensities are crucial for tify adjustments in Pn, Amax, Fv/Fm, Gs, WUE, ETR,
optimizing field cultivation and management practices. and NPQ in response to seasonal variations in solar illu-
Light is a key environmental signal that triggers chlo- mination and tillage management, as citrus leaves release
rophyll (Chl) biosynthesis and induces variable pho- significant amounts of CO2 and water. ETR is a rapid
tosynthetic responses based on changes in irradiance method to assess the photosynthetic capacity of citrus
(Wang et al. 2021). Chlorophyll fluorescence (ChlF) is under light intensity stress (Chen et al. 2021). It allows for
a noninvasive technique that accurately measures the simple evaluations of photosynthesis and estimations of
functioning of photosynthetic apparati in plants and is the relationships between heat quenching and photosyn-
frequently used to investigate plant responses to various thetic efficiency. Variable photosynthesis parameters are
environmental stresses, both in controlled environments sensitive indicators of the physiological status of tested
and in the field (Kałuzewicz et al. 2018). ChlF values can plants and provide a quick means to identify their physi-
provide insights into several aspects of photosynthesis, ological condition (Wang et al. 2021).
including the potential for photosynthesis, photochemi- Therefore, we hypothesized that the photosynthetic
cal dissipation, the percentage of photosystem II (PSII) characteristics would exhibit significant differences
that is open, the effectiveness of PSII in capturing photo between CA and SC over varied seasons and photosyn-
energy from light-harvesting complexes, and the subse- thetic photon flux densities (PPFD) in tea fields. The
quent transfer of quanta (Moya et al. 2019). Variations in objectives of this study were to clarify the effects of tillage
light intensity directly impact ChlF values in tea plants, and seasonal dynamics on the photosynthetic apparatus
enabling the assessment of the status of their photosyn- of tea plants by measuring their photosynthetic capacity
thetic apparatus and photoreceptors. This internal physi- and ChlF parameters in response to varying light intensi-
ological response is recorded as a photosynthetic index, ties. Understanding these effects will allow us to evaluate
which includes variables such as stomatal conductance seasonal physiological changes in tea plants and provide
(Gs), net photosynthetic rate (Pn), dark respiration rate
Chen et al. Botanical Studies (2024) 65:10 Page 3 of 12

tools for improving photosynthetic productivity and canopy were dark-adapted for 30 min by the use of leaf
planting management patterns of tea plants. clips. Following this, the central region of the adaxial
leaf surface was subjected to a saturating light pulse of
Materials and methods 3,500 μmol m− 2 s− 1 (690 nm) prior to being measured.
Site description, experimental field management, and Analysis of photosynthetic capacity and ChlF param-
experimental design eters have been described in our previous paper (Chen
Tea plants [Camellia sinensis L. O. Kuntze cv. TTES et al. 2021). Briefly, Fv/Fm and ΦPSII were calculated as
No.12 (Jhinhsuan)] 45–55 cm tall and more than 20 years (Fm - Fo) / Fm and (Fm’ - Fo’) / Fm’, respectively. Fo (Fo’)
old were grown in two experimental fields, one under CA and Fm (Fm’) are the minimal and maximal fluorescence
(120°39’12.4”E, 23°38’36.7”N, Figure S1A) and the other values of dark-adapted and during-illumination leaves,
under SC (120°39’06.2"E, 23°38’26.3"N, Figure S1B) at respectively. Values of the Fo and Fm of the dark-adapted
certified organic plantations grassland covers more than samples were determined, and gas exchange and ChlF
80% of the area (Liu et al. 2021). CA and SC practices for measurements were simultaneously measured at 10:00
controlling soil and water losses were similar from June, a.m. on a clear day under the stable environmental con-
2019, to May, 2020. Both plantations are located in a low- ditions of the leaf chamber. Environmental conditions
elevation (ca. 400 m) mountainous area of central Taiwan during the experiment were set to a gas-flow rate at 750
where the climate is humid subtropical. Mean annual μmol s–1, gas-mixer speed to level 7, assimilator tempera-
rainfall of 2,500 mm and mean annual air temperature of ture to 25°C, and relative humidity to 75%. ΔF/Fm’ was
24.5 °C were recorded from June 2019 to May 2020 (Fig- calculated as (Fm’ - F) / Fm’. ETR was obtained as ΔF/
ure S2). The world reference base for soil resources classi- Fm’ x PPFD x 0.5 × 0.84. NPQ was calculated as (Fm/Fm’)
fies its soil as a typical andosol in which the texture of the -1. Moreover, Rd (μmol CO2 m− 2 s− 1), Qy (CO2/ PPFD),
upper surface is sandy loam. and LCP (μmol PPFD m− 2 s− 1) were obtained from the
The experiment took place in the two agricultural sys- linear regression of photosynthetic light response curves
tems over four seasons (spring was from March to May, to illumination measured from 0 ∼ 100 μmol PPFD m− 2
summer was from June to August, fall was from Sep- s− 1. Values for Pn and Gs were simultaneously calculated
tember to November, and winter was from December to and recorded inside the chamber of the photosynthesis
February), with each cover crop treatment having four analyzer (GFS-3000FL, Walz, Effeltrich, Germany). The
replications. The cover crops were Paspalum conjuga- operation was automatic, and data were stored in the
tum Berg., Cynodondactylon (L.) Pers., Wedelia chinen- computer within the console and analyzed. All measure-
sis Merr., and Bidens pilosa var. pilosa. CA fields were ments were performed on fifteen leaves (the second to
cropped with a flail mower in the first week of each sea- third mature leaves) from five replicates for each treat-
son, with residues being left on the soil surface for nutri- ment of 380–400 ppm in the atmospheric environment at
ent supply. Organic cultivation methods were performed, room temperature (25 °C) from mid-morning until mid-
including no chemical fertilizers or herbicides being used afternoon (10:00 ∼ 17:00).
during the experiment. No severe pests or diseases were
encountered during the experiments. A completely ran- Statistical analysis
domized design employing the two no-tillage methods The gas exchange of plant response to different illumi-
and four seasonal treatments was used, and there were nation intensities was recorded by the instrument after
five replicates per treatment. For each treatment, five 5–10 min equilibrium in the chamber and three rep-
intact, fully expanded leaves (the second to third mature lications were averaged to presnt in the figure. Statis-
leaves) and leaf samples were randomly sampled from tical analyses were performed using PASW Statistics
robust and healthy plants at the end of each season. 18 software (PASW 18, IBM, USA). Gas exchange and
ChlF measurements were analyzed using a single-factor
Determination of photosynthetic capacityand ChlF analysis of variance (ANOVA) to check for significant
parameters with a fixed light source differences between CA and SC, and differences among
In all seasons, PPFD was adjusted to 0, 5, 10, 15, 25, 50, season means were assessed using Tukey’s HSD test with
75, 100, 200, 400, 800, 1200, 1500, 1800, and 2000 μmol p < 0.05 significance. In addition, two-way ANOVA was
photon m− 2 s− 1 in a leaf chamber for 75 min to under- used for the interaction of tillages and seasons. Multiple
stand how radiant energy was used by the tested plants comparisons were performed using the least-significant
under different illumination intensities. Plants were difference. Regression analyses were used to examine
measured with a gas-exchange and fluorescence photo- relationships between Gs and Pn and among ETR, Pn,
synthesis analyzer (GFS-3000FL, Walz, Effeltrich, Ger- and NPQ. In addition, model datasets were based on at
many) from June 2019 to May 2020. The second to third least 25 leaves (the second to third mature leaves) from
mature leaves (one bud and two leaves) of each plant’s each PPFD level, and ChlF parameters were calculated
Chen et al. Botanical Studies (2024) 65:10 Page 4 of 12

using ETR data from the model validation datasets. decrease in ΔF/Fm’ (%) in all seasons, followed by stabi-
Several models were tested, including linear regression lization from 1,500 to 2,000 PPFD (Fig. 1I, J). Under CA,
models being selected for the interpretation of the rela- spring and fall ΔF/Fm’ and Fv/Fm (%) from 200 to 2,000
tionship between ChlF parameters and PPFD. All mod- PPFD were significantly higher than in summer (Fig. 1I).
els were evaluated for goodness of fit by the graphical Conversely, under SC, spring ΔF/Fm’ and Fv/Fm (%)
analysis of residuals and by computing correlation coef- from 200 to 400 PPFD and 800-2,000 PPFD were signifi-
ficients at a significance level of p < 0.05 between the gas- cantly lower and higher, respectively, than in fall (Fig. 1J).
exchange and ChlF parameters. The linear regression Table 2 presents the variations in Rd, Qy, LCP, Amax,
model performance proved more suitable. and Fv/Fm of tea mature leaves over eight seasons under
two tillages. Regardless of the season, all Rd values in CA
Results (1.23 ∼ 1.86 μmol CO2 m− 2 s− 1) were significantly higher
The impact of two cultivation methods and four sea- than in SC (0.57 ∼ 1.03 μmol CO2 m− 2 s− 1). Under both
sons on tea photosynthetic parameters (Pn, Gs, slope tillage methods, Qy significantly increased in spring
of Gs-Pn, ETR, NPQ, ΔF/Fm’, Fv/Fm, Rd, Qy, LCP, and (0.04 CO2/PPFD) compared to other seasons (0.02 ∼ 0.03
Amax) under 2,000 PPFD is presented in Table 1. Except CO2/PPFD), suggesting that the relative increase in
for Rd in seasons and Fv/Fm in T x S, all photosynthetic CO2 and carbon sink behavior may be a response to
indices exhibited significant differences (p < 0.0001, 0.001, physiological acclimation in spring. CA exhibited sig-
0.05, and 0.01) in both main and interaction effects. Fur- nificantly higher LCP values (39.88 ∼ 61.10 μmol PPFD
thermore, Fig. 1 indicates that, under 0-100 PPFD, no m− 2 s− 1) compared to SC (11.66 ∼ 35.05 μmol PPFD
significant seasonal differences in any photosynthetic m− 2 s− 1) across seasons in both tillage methods. More-
parameters were observed in either tillage. However, for over, regardless of the tillage method, Amax values sig-
200-2,000 PPFD, spring Pn values were notably higher nificantly increased in the order of spring, summer, fall,
than in other seasons, regardless of tillage (Fig. 1A, B), and winter. Similarly, Fv/Fm levels significantly increased
except for 200 PPFD under CA, where no significant sea- in spring (0.76) compared to other seasons (0.73 ∼ 0.75)
sonal differences in Pn values were noted (Fig. 1A). As under both tillage methods.
light intensity escalated, Pn values under CA rose from 0 Figure 2 illustrates the significant impact of light inten-
to 1,500 PPFD across all seasons, then gradually declined sity (ranging from 0 to 2,000 PPFD) and seasonal varia-
(Fig. 1A), whereas under SC, Pn significantly increased tion on the correlations between stomatal conductance
in the order of winter, fall, summer, and spring (Fig. 1B), (Gs) and net photosynthetic rate (Pn) in tea plants under
indicating seasonal Pn responses to all light intensities. two different tillages, CA and SC In both fall and win-
Spring Gs content under CA significantly surged from ter and spring and summer under CA, there were posi-
200 to 1,200 PPFD compared to other seasons (Fig. 1C), tive and significant correlations between Gs and Pn with
whereas under SC, Gs values decreased significantly from r² values of 0.996 and 0.8, respectively (Fig. 2A). Similar
spring to winter across 200-2,000 PPFD (Fig. 1D). Spring significant positive correlations were observed under
ETR levels were significantly higher than other seasons SC, with r² values of 0.8 and 0.829 for fall and winter and
from 400 to 2,000 PPFD, and ETR for both tillages consis- spring and summer, respectively (Fig. 2B). Interestingly, a
tently rose from 0 to 1,200 PPFD, then declined (Fig. 1E, higher slope in the Pn/Gs linear relationship, equivalent
F). Figure 1G and H show that, regardless of tillage, fall to WUE, was detected in fall and winter under SC (0.144)
and winter NPQ values from 400 to 2,000 PPFD were sig- compared to CA (0.122 and 0.123), indicating higher
nificantly higher than in spring, and NPQ increased in all photosynthesis in SC treatments.
mature leaves, seasons, and tillages as light intensity rose Figure 3 depicts the relationships among ETR, Pn, and
from 0 to 2,000 PPFD. However, as light intensity rose NPQ of plants under CA and SC across four seasons at
from 0 to 1,200 PPFD, both tillages exhibited a steady light intensities ranging from 0 to 1,200 μmol m− 2 s− 1

Table 1 ANOVA of tillage (T), season (S), and their interactions (T x S) for Pn, Gs, slope of Gs-Pn, ETR, NPQ, ΔF/Fm’ (%), Fv/Fm, Rd, Qy,
LCP, and Amax of tea plants at 2,000 μmol m− 2 s− 1 PPFD under CA and SC in four seasons
F-value and significance
Source of variance Pn Gs Slope ETR NPQ ΔF/Fm’ (%) Fv/Fm Rd Qy LCP Amax
Tillage (T) 457.66 376.08 39.03 4.70 26.82 67.84 26.89 58.93 54.57 181.46 305.79
**** **** **** * **** **** **** **** **** **** ****
Season (S) 428.50 1038.31 13.24 67.30 44.44 108.02 14.70 2.014 66.11 15.31 370.91
**** **** **** **** **** **** **** NS **** **** ****
T×S 93.39 81.00 5.19 4.64 13.46 9.98 0.46 8.23 4.57 7.45 84.38
**** **** ** ** **** **** NS *** ** ** ****
Chen et al. Botanical Studies (2024) 65:10 Page 5 of 12

Fig. 1 Comparison of conventional agriculture and sod culture on Pn, Gs, ETR, NPQ, ΔF/F’m, and Fv/Fm of tea plants grown in four seasons (●=spring,
▼=summer, ■=fall, ◆=winter, The solid ones are CA and the hollow ones are SC.) monitored from June 2019 to May 2020. Data are mean ± standard
error, and each point represents the mean of five mature leaves. Different letters indicate significant differences in Tukey’s HSD analyses over four seasons
(p < 0.05)
Chen et al. Botanical Studies (2024) 65:10 Page 6 of 12

Table 2 Influence of CA and SC on Fv/Fm, Rd, Qy, LCP, Amax, and Fv/Fm of tea plants grown in four seasons monitored from June
2019 to May 2020
Photosynthetic parameters Conventional agriculture (CA) Sod culture (SC)
Spring Summer Fall Winter Spring Summer Fall Winter
Rd 1.86a 1.23c 1.49b 1.28c 0.57f 0.76e 1.03d 1.03d
(μmol CO2 m− 2 s− 1)
Qy 0.04a 0.03b 0.02c 0.02c 0.04a 0.03b 0.03b 0.03b
(CO2/ PPFD)
LCP 49.38c 39.88d 61.10a 54.03bc 11.66f 24.17e 27.88e 35.05d
(μmol PPFD m− 2 s− 1)
Amax 10.43b 8.05cd 6.46e 6.16e 18.82a 9.85b 8.36cd 7.16d
(μmol CO2 m− 2 s− 1)
Fv/Fm 0.76a 0.74c 0.74c 0.73d 0.76a 0.75b 0.75b 0.75b
Means followed by same letter within rows of eight seasons under CA and SC methods are not significantly different according to Tukey’s HSD analyses (p < 0.05).
Each point represents the mean of 5 mature leaves

Fig. 2 Correlations between the Gs and Pn of tea grown under conventional agriculture (panel A) and sod culture (panel B) in four seasons (●=spring,
▼=summer, ■=fall, ◆=winter, The solid ones are CA and the hollow ones are SC.) monitored from June 2019 to May 2020. Plants were subjected to
light irradiations of 0, 5, 10, 15, 25, 50, 75, 100, 200, 400, 800, 1,200, 1,500, 1,800, and 2,000 μmol m− 2 s− 1 PPFD for 75 min. Each symbol represents the
average of five mature leaves on one plant, and five plants were randomly selected for tillage and season treatments. Each line represents the time point
of 48 values (two seasons multiplied by 15 PPFD) from the model’s validation datasets. The correlation coefficients (r) are calculated and significance (p)
is at the 0.0001 probability (*****) level

PPFD. Significant correlations were found between ETR observed in spring compared to other seasons under both
and Pn (r² = 0.977 and 0.945 for CA and SC, respectively; tillage methods, indicating a stronger non-photochemi-
Fig. 3A, B) and between ETR and NPQ (r² = 0.772 and cal dissipation ability in spring relative to other seasons.
0.636 for CA and SC, respectively; Fig. 3C, D) under the
same PPFD conditions and seasons. Discussion
Figure 4 illustrates the correlations among ETR, Pn, The ChlF components of tea plants were utilized to assess
and NPQ in tea grown under CA and SC at higher light various functional levels of photosynthesis induced by
intensities (1,200 to 2,000 μmol m− 2 s− 1 PPFD). ETR was light intensities and tillage methods. Figure 1 demon-
significantly and positively correlated with Pn under both strates that, at light intensities ranging from 800 to 2,000
CA and SC (r² = 0.843 and 0.969, respectively; Fig. 4A, B), PPFD in spring, the values of net Pn, Gs, ETR, and ΔF/
indicating notably higher Pn values in spring under SC Fm’ and Fv/Fm (%) for SC were comparatively higher
compared to CA. This suggests a stronger photosynthe- than those for conventional agriculture (CA), while NPQ
sis rate in SC mature leaves during spring. Conversely, values for SC were relatively lower than those for CA.
ETR values were significantly and negatively correlated This suggests that SC experienced less photoinhibition
with NPQ (r² = 0.559 and 0.873 for CA and SC, respec- in spring, maintaining high photochemical efficiency
tively; Fig. 4C, D). Additionally, higher NPQ values were and photosynthesis rates. With increasing light intensity,
Chen et al. Botanical Studies (2024) 65:10 Page 7 of 12

Fig. 3 Correlations among ETR and Pn, NPQ of tea plants grown under conventional agriculture (panels A, C) and sod culture (panels B, D) in four sea-
sons (●=spring, ▼=summer, ■=fall, ◆=winter, The solid ones are CA and the hollow ones are SC.) monitored from June 2019 to May 2020. Plants were
subjected to light irradiances at 0, 5, 10, 15, 25, 50, 75, 100, 200, 400, 800, and 1,200 μmol m− 2 s− 1 PPFD for 60 min. Each symbol represents the average
of five mature leaves on one plant, and five plants were randomly selected from tillage and season treatments. Each line represents the time point of 48
values (four seasons multiplied by 12 PPFD) from model validation datasets. Correlation coefficients (r) are calculated and significance (p) is at the 0.0001
probability (*****) level

higher ETR values during spring correlated with higher Wong et al., 2016; Demmig-Adams et al. 2020). There-
photosynthetic efficiency compared to other seasons, fore, higher Pn, Gs, and ETR values detected in spring
suggesting that tea plants adapt to high light intensi- than in other seasons might be caused by younger leaves
ties in spring. Furthermore, when light intensity was in spring. Additionally, the average high temperatures of
maintained below 1,500 PPFD, Pn, Gs, ETR, and NPQ 35 °C in summer and 30 °C in fall in Taiwan may contrib-
all increased simultaneously, indicating that excess light ute to higher NPQ performances (Fig. 1G, H) and lower
energy potentially dissipated via heat quenching, and that Pn levels (Fig. 1A, B) for both CA and SC compared to
there exists an optimal light intensity (1,200-1,500 PPFD) spring. Generally, high temperature and high light inten-
for tea plant growth. sity negatively affect photosynthetic capacity, and high
Comparatively lower NPQ levels were observed in temperatures usually coincide with high light intensities.
both CA and SC during spring (Fig. 1G,H), while Pn In photosynthetic organisms, elevated irradiance lev-
at 1,200-1,500 PPFD was highest, reaching 10.4 μmol els during environmental stress conditions, such as high
CO2 m− 2 s− 1 for CA and 18.1 μmol CO2 m− 2 s− 1 for temperatures, frequently lead to photoinhibition, char-
SC (Fig. 1A,B). This implies that higher photosynthesis acterized by a reduction in photosynthetic activity (Pn).
rates consume more light energy, reducing excess light This phenomenon occurs due to the surplus light energy
energy, and, consequently, resulting in lower NPQ and exacerbating the generation of detrimental reactive oxy-
photoinhibition (Fig. 1I, J) (Demmig-Adams et al., 2006; gen species within the chloroplasts (Endo et al. 2023).
Chen et al. Botanical Studies (2024) 65:10 Page 8 of 12

Fig. 4 Correlations among ETR and Pn, NPQ of tea plants grown under conventional agriculture (panels A, C) and sod culture (panels B, D) in four sea-
sons (●=spring, ▼=summer, ■=fall, ◆=winter, The solid ones are CA and the hollow ones are SC.) monitored from June 2019 to May 2020. Plants were
subjected to light irradiances at 1,200, 1,500, 1,800, and 2,000 μmol m− 2 s− 1 PPFD for 20 min. Each symbol represents the average of five mature leaves
on one plant, and five plants were randomly selected from tillage and season treatments. Each line represents the time point of 16 values (four seasons
multiplied by 4 PPFD) from model validation datasets. Correlation coefficients (r) are calculated and significance (p) is at the 0.0001 probability (*****) level

PSII is often the most sensitive component of the photo- 60%) observed at 800 to 2,000 PPFD, and the reduced Pn
synthetic apparatus to high temperatures or light inten- (Fig. 1A, B) and ETR (Fig. 1E, F) levels observed at 1,800
sities and is susceptible to photodamage (Pospíšil, 2016; to 2,000 PPFD, indicate the presence of photoinhibition.
Gao et al., 2019). This susceptibility may lead to higher Regardless of the season or cultivation method, a light
photoinhibition (Murata et al., 2007; Zulfugarov et al. intensity ranging from 800 to 1,500 PPFD was deemed
2007; Tikkanen et al., 2014) and lower Pn (Molina-Bravo optimal for plant growth. Thus, management strategies
et al. 2011) in tea plants during summer and fall. for tea plants should aim to mitigate the effects of high
Increasing light intensity was associated with a rise in temperatures and intense light during summer and fall,
NPQ and a decline in ΔF/Fm’ (Fv/Fm) across all seasons for instance, by spraying water in the afternoon or using
and cultivations (Fig. 1I, J), suggesting that both tillage the surrounding terrain and trees to shield against exces-
methods resulted in low photosynthetic rates, necessitat- sive incident light, ultimately enhancing tea leaf pro-
ing the dissipation of excess energy to safeguard the PS. duction and quality. Moreover, SC outperformed CA
At light intensities of 1,200 to 2,000 PPFD, NPQ and ΔF/ as SC bolstered soil organic matter content, augmented
Fm’ (Fv/Fm) values were consistently maintained at high soil water-holding capacity, and ameliorated the garden
and low levels, respectively, with minimal or no variation, microclimate (Bai et al. 2017; Lin et al., 2019), thereby
signifying that their photochemical capacity had reached rendering SC more resilient to the climatic extremes
a plateau. The diminished ΔF/Fm’ (Fv/Fm) levels (below associated with climate change.
Chen et al. Botanical Studies (2024) 65:10 Page 9 of 12

In Table 2, the Rd and LCP values under CA were sig- of tea plants was not restricted during suitable tempera-
nificantly higher than those under SC, potentially due tures, resulting in higher Pn and a more efficient water-
to the long-term tillage cropping system and the year- use strategy developed in response to spring and summer
round reduction in soil moisture content (Dominika conditions. CA exhibited lower water efficiency in spring
et al. 2020) at the study sites, which subsequently led and summer due to the ease of surface water evapotrans-
to reduced foliar respiration, growth rates, and carbon piration, which led to reduced Pn. Despite the presence
accumulation potential (Chen et al. 2021). This relative of a sprinkler irrigation system in the field, water short-
water deficit might have induced a drought-like state in ages were encountered, particularly during the absence of
CA-treated tea plants, resulting in elevated Rd and LCP rainfall in spring and summer throughout the experimen-
values. In contrast, the ground surface cover in the SC tal period. The elevated Pn and Gs in spring and summer
conservation agricultural system likely mitigated water might also be attributed to the new leaves being well-
evaporation, enhanced WUE, improved leaf morphol- suited to the temperatures. Gs levels under CA were con-
ogy and photosynthetic properties, increased soil organic sistently lower than those under SC in each season, which
content, and boosted carbon sequestration, especially in might have constrained tea leaf photosynthesis, placing
the soil surface layer. Notably, the levels of Qy, Amax, and CA in a potentially water-stressed condition. Since pho-
Fv/Fm in mature leaves during spring were significantly tosynthesis, CO2, and water are pivotal for plant growth
higher than in other seasons, suggesting that the precipi- and yield, plants must strike a balance between CO2
tation and temperature in spring were favorable for tea uptake for photosynthesis and water loss through tran-
plant growth. Specifically, CA employed an automatic spiration. Stomata regulate gas exchange between the
watering system, whereas SC relied solely on natural leaf interior and external atmosphere, thereby enhanc-
precipitation for water supply. The photosynthetic light ing WUE (Deans et al. 2018; Eyland et al. 2021). ETR
response curve not only illustrated the expected relation- exhibited significant and positive correlations with Pn
ship between light intensity and leaf Pn but also indicated and NPQ when exposed to 0 ∼ 1,200 PPFD (Fig. 3) and
that the calculated parameters LCP, Amax, and Rd could 1,200 ∼ 2,000 PPFD (Fig. 4A, B), whereas significant
be employed to assess the impact of soil conditions and and negative correlations were observed between ETR
climatic factors on plants (Lachapelle et al., 2012; Lang and NPQ at high illuminations of 1,200 ∼ 2,000 PPFD
et al. 2013; Chen et al. 2018). These parameters are also (Fig. 4C, D). These results suggest that photochemical
linked to metabolic changes that can be utilized to pre- and non-photochemical quenching would concurrently
dict the effects of future climate change on plant pro- up-regulate Pn at 0 ∼ 1,200 PPFD. Photoinhibition might
ductivity (O’Leary et al., 2017). In our study, Rd, Qy, occur when tea plants are intolerant to high light, and the
LCP, Amax, Fv/Fm, ΔF/Fm’, Pn, Gs, ETR, and NPQ were elevated photosynthesis in spring could be attributed to
found to be appropriate for evaluating photosynthetic its temperature factor. However, at 1,800 ∼ 2,000 PPFD,
efficiency. Over time, SC is likely to enhance biodiversity photoinhibition occurred in PSII), leading to decreased
(Trifonova et al. 2022), optimize the microclimate (Liu et photochemical efficiency, ETR, and Pn. As a result, tea
al. 2021), and lead to improved Qy, LCP, Amax, and Fv/ plants might be experiencing high-illumination stress,
Fm in mature leaves exposed to varying light levels. Con- causing a reduction in ETR (Fig. 1E, F). Nevertheless, the
sequently, SC could bolster the resilience of tea fields to excess light energy generated would consequently main-
climate change, thereby sustaining tea production and tain NPQ at 1,200 ∼ 2,000 PPFD (Fig. 2G, H) due to the
economic revenue. SC may be particularly advantageous continuous photoprotective mechanism maintained by a
for ecosystems with uneven rainfall distribution. high proportion of NPQ as illumination increased.
The comparison between CA and SC across differ- The photosynthetic parameters analyzed in this study
ent seasons serves as a valuable tool for evaluating the are highly sensitive indicators that enable quick identifi-
impacts of global climate change and its applicability to cation of the physiological status of plants (Hirotsu et al.
the physiological states of crops. Throughout all seasons 2005). Specifically, ΔF/Fm’ (Fv/Fm) represents the pho-
and light illuminations, the photosynthesis curves of CA tosynthetic potential for photochemical dissipation, and
and SC displayed positive and significant correlations the photochemical ability of photosystem II (PSII) under
between Pn and Gs (Fig. 2), indicating that the increase various light intensities exhibits a linear relationship
in Pn might be attributed to stomatal opening, which in with the CO2 fixation rate (Cui et al. 2006). High irradia-
turn limits the reduction of photosynthetic rates. During tion exposure may significantly depress ΔF/Fm’ (Fv/Fm),
the photosynthesis saturation period, changes in Pn were leading to the suppression of the electron transfer chain
primarily influenced by Gs, subsequently leading to the (Wu et al. 2015). The ETR is valuable for non-destruc-
maintenance of high WUE. Generally, Gs levels in spring tively estimating net photosynthesis rate (Pn) and NPQ,
and summer were significantly higher than those in fall thus simplifying evaluations of the relationship between
and winter, suggesting that the stomatal opening speed heat dissipation and photosynthetic efficiency. These
Chen et al. Botanical Studies (2024) 65:10 Page 10 of 12

parameters are expected to exhibit quantifiable differ- Supplementary Information

ences between CA and SC tea plant cultures under vari- The online version contains supplementary material available at https://doi.
org/10.1186/s40529-024-00416-0.
ous seasons and light intensities. Moreover, these metrics
should be capable of indicating how controlled light Supplementary Material 1
intensities might be utilized to enhance rapid, large-scale,
and precise commercial management of tea plants. Given Author contributions
that ΔF/Fm’ (Fv/Fm) encompasses all these parameters, Chung-I Chen. and Ching-Wen Wang designed the experiments, Kuan-
its use is recommended across all tea regions for evalu- Hung Lin and Chung-I Chen wrote the paper; Meng-Yuan Huang, Chih-Kai
Yang, Yu-Hsiu Lin, Mei-Li Hsueh and Li-Hua Lee conducted experiments
ating tea plants in terms of radiation use efficiency and and analyzed the data. Shiou-Ruei Lin and Ching-Wen Wang visualized and
photosynthetic system status. Understanding the photo- supervised the study. All authors have read and agreed to the published
synthetic characteristics of tea plants under different sea- version of the manuscript.
sons and tillage methods, through remote sensing of their Funding
physiological state, would undoubtedly inform field cul- This work was financially supported by the Council of Agriculture, Executive
tivation management. For example, optimizing field till- Yuan and Ministry of Science and Technology of Taiwan.
age methods and implementing artificial shading could Data availability
help avoid photoinhibition factors that are anticipated The data and materials are available upon reasonable request from the
to intensify due to global climate change. Such remote corresponding author.
sensing is expected to be particularly beneficial in fields Code availability
experiencing seasonal aridity during cycles of prolonged Not applicable.
drought and heavy rain.
Declarations
Conclusions
Ethics approval
The positive effects of SC on Amax, Fv/Fm, Gs, WUE, Not applicable.
ETR, and NPQ suggest that SC is advantageous for
the production and drought resistance of tea plants Consent to participate
Not applicable.
under future climate change scenarios. Quantifying the
responses of Pn, Amax, Fv/Fm, Gs, WUE, ETR, and NPQ Consent for publication
to seasonal light variations is crucial for developing indi- Not applicable.
cators for tillage management. Utilization of parameters Conflict of interest
such as Amax, WUE, ETR, and NPQ not only facilitates The authors declare that there is no competing interest and that the article
the rapid assessment of the photosynthetic capacity of tea is submitted without any commercial or economic interest that could be
generated as a potential conflict of interest.
plants across four seasons, taking into account responses
to factors like light intensity, drought, and temperature, Received: 23 September 2023 / Accepted: 18 February 2024
but also allows for accurate field management aligned
with the environmental benefits of SC. This approach
provides a tea garden management model that addresses
the impacts of climate change. References
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