Published online August 25, 2023
Journal of Ecology and Environment (2023) 47:09
1Department of Integrative Natural Sciences for the East Sea Rim, Kyungpook National University, Daegu 41566, Republic of Korea
2Department of Biology, Kyungpook National University, Daegu 41566, Republic of Korea
3Research Institute for Dok-do Ulleung-do Island, Kyungpook National University, Daegu 41566, Republic of Korea
4Seed Vault Center, Baekdudaegan National Arboretum, Bonghwa 36209, Republic of Korea
Correspondence to:Yeon-Sik Choo
†These authors contributed equally to this work.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Background: Ecophysiological characteristics of Rosa rugosa were analyzed under different environmental factors from May to October 2022. Photosynthesis, chlorophyll fluorescence, chlorophyll content, leaf water content (LWC), osmolality, carbohydrate content, and total ion content were measured to compare the physiological characteristics of R. rugosa at two study sites (i.e., in large pots and in the Goraebul coastal sand dune area).
Results: When R. rugosa was exposed to high temperatures, photosynthetic parameters including net photosynthetic rate (PN) and stomatal conductance (gs) in both experiment areas declined. In addition, severe photoinhibition occurs when R. rugosa is continuously exposed to high photosynthetically active radiation (PAR), and because of this, relatively low Y(II) (i.e., the quantum yield of photochemical energy conversion in photosystem II [PSII]) and high Y(NO) (i.e., the quantum yield of non-regulated, non-photochemical energy loss in PSII) in the R. rugosa of the pot were observed. As the high Y(NPQ) (i.e., the quantum yield of regulated non-photochemical energy loss in PSII) of R. rugosa in the coastal sand dune, they dissipated the excessed photon energy through the non-photochemical quenching (NPQ) mechanism when they were exposed to relatively low PAR and low temperature. Rosa rugosa in the coastal sand dune has higher chlorophyll a and carotenoid content. The high chlorophyll a + b and low chlorophyll a/b ratios seemed to optimize light absorption in response to low PAR. High carotenoid content played an important role in NPQ. As a part of the osmotic regulation in response to low LWCs, R. rugosa exposed to high temperatures and continuously high PAR used soluble carbohydrates and ions to maintain high osmolality.
Conclusions: We found that Fv/Fm was lower in the potted plants than in the coastal sand dune plants, indicating the vulnerability of R. rugosa to high temperatures and PAR levels. We expect that the suitable habitat range for R. rugosa will shrink and move to north under climate change conditions.
Keywords: climate change, coastal sand dune, environmental change, photosynthesis, Rosa rugosa
Plants are exposed to various environmental factors throughout their life span due to their sedentary life. Environmental factors are divided into several categories, including pathogen infection, biotic stress (e.g., herbivory), and abiotic stress (e.g., drought, high temperature, nutrient deficiency, and exposure to salt or heavy metals; Suzuki et al. 2014). Of these factors, abiotic stress is a major threat to plants that limits their growth and distribution and should be overcome (Rajaniemi and Allison 2009; Rajkumar et al 2017; Thakur and Nayyar 2013). The intensity and frequency of abiotic stress varies with habitat. In coastal sand dune habitats, abiotic stresses include temperature, light intensity and duration, wind, wind-driven sand movement, and salinity, all of which occur at a higher intensity and frequency than in other habitats (Frosini et al. 2012). These stresses induce ionic imbalances in plant tissues and lead to decreased photosynthetic efficiency due to reduced enzyme activities (e.g., rubisco) and increased leaf respiration rates (Allakhverdiev et al. 2008; Chang et al. 2020; Medina and Francisco 1997; Sudhir and Murthy 2004). Furthermore, stress-generated reactive oxygen species (ROS) induce negative effects, such as oxidative damage in plant tissues (Chang et al. 2020; Singh and Thakur 2018).
Various abiotic stresses combine in outdoor environments to affect plants (Billings 1952; Suzuki et al. 2014). The effects of such combined abiotic stresses on plants are limited to the plant’s response to a single stressor, since plants utilize specific mechanisms in response to abiotic stresses that are dependent on specific stress combinations in addition to their unique response mechanisms for single stresses (Suzuki et al. 2014). The metabolic and signaling responses of plants to multiple stresses are highly diverse and include photosynthesis, osmolytes synthesis, and hormonal signaling mechanisms (Iyer et al. 2013; Prasch and Sonnewald 2013; Suzuki et al. 2014). However, these mechanisms remain poorly understood.
Among the components of a plant, the leaf is the primary organ where photosynthesis, the key process that converts light energy from photons into chemical energy usable by the plant, takes place. Leaves are also recognized as a representative organ that can be used to assess physiological traits, including plant growth and adaptation, can be assessed (Ashraf and Harris 2013; Givnish 1987; Hohmann-Marriott and Blankenship 2011). Photosynthesis occurs through a complex interaction of structures (e.g., photosystem II [PSII], PSI, and cytochrome b6f complex) and enzymes (e.g., rubisco and ATP synthase) inside chloroplast thylakoids (Allen et al. 2011; Ashraf and Harris 2013; Jensen and Leister 2014). In particular, PSII and the light harvest complex (LHC) catalyze water oxidation and harvest and convert photons to electronic energy to initiate photosynthesis (Albanese et al. 2020; Kawakami and Shen 2018). Since PSII is affected by a wide range of environmental factors, including moisture, temperature, and day length, there has been great interest in the relationship between photosynthetic capacity and PSII activity to obtain a better understanding of how plants respond to their environment (Adams and Langton 2005; Ashraf and Harris 2013; Villar et al. 2006). Abiotic stresses often cause osmotic pressure changes within plants, to which lead plants to respond by utilizing osmolytes such as soluble carbohydrates and ions (Vicente et al. 2016). Soluble carbohydrates are products of photosynthesis and are known to be primarily involved in osmotic pressure regulation (Gil et al. 2013; Singh and Thakur 2018). Thus, the accumulation of osmolytes can be assessed to understand how plants respond to abiotic stresses (Chapin et al. 1990).
The inability of plants to respond appropriately to abiotic stresses results in photoinhibition, which limits photosynthesis and the activity of the plant’s photosynthetic machinery. Photoinhibition causes photon energy to be captured rather than absorbed, leaving the remaining energy as a potential threat to the PS, especially PSII (Takahashi and Badger 2011). Plants have developed photoprotective mechanisms to overcome photoinhibition, prevent the inactivation of PSII, restore an already closed PSII to an active state (Takahashi and Badger 2011). Various morphological and physiological characteristics of plants are involved in photoprotection, including non-photochemical quenching (NPQ) mechanisms that utilize carotenoids, such as xanthophylls, and D1 protein reconstitution (Kitao et al. 2000).
This study aimed to investigate the physiological and ecological characteristics of
The environmental factors measured were leaf temperature, vapor pressure deficit based on leaf (VPDL) temperature (kPa), soil moisture content (%), and photosynthetically active radiation (PAR) (
Meteorological data for the period May–October 2022 at the Kyungpook National University, where the research tree species is located, and at Goraebul coastal sand dunes, Yeongdeok-gun, Gyeongsangbuk-do, Republic of Korea, are presented in terms of daily average temperature (°C), daily maximum temperature (°C), and daily minimum temperature (°C), relative humidity (%), daily precipitation (mm), maximum instantaneous wind speed (m/s), maximum wind speed (m/s), and average wind speed (m/s). These data were collected from the Korea Meteorological Administration Longitudinal Observation Data.
A portable photosynthesis meter (Li-Cor 6400) was used to measure photosynthetic metrics. For accurate measurements, a reference CO2 concentration of 400
Chlorophyll fluorescence was measured using a portable chlorophyll fluorometer (PAM-2500; Heinz Walz GmbH, Pfullingen, Germany) to determine Y(II) (i.e., the quantum yield of photochemical energy conversion in PSII), Y(NPQ) (i.e., the quantum yield of regulated non-photochemical energy loss in PSII), and Y(NO) (i.e., the quantum yield of non-regulated, non-photochemical energy loss in PSII) in fully grown leaves exposed to light. After a dark adaptation period of more than 25 minutes, the minimum fluorescence yield of the dark-adapted state (Fo) and the maximum fluorescence yield of the dark-adapted state (Fm) were measured, and the Fv/Fm ratio (i.e., the maximum photochemical quantum yield of PSII) was calculated using the formula (Fm − Fo) / Fm.
Leaf temperature, VPDL, and PAR were measured using a portable photosynthesis measuring device (Li-Cor 6400) in large pots at Kyungpook National University in June and August 2022, and in the corresponding dune at Goraebul coastal dunes in August 2022. Soil moisture content was measured using a soil moisture meter (Theta Probe ML3).
To measure the diurnal variations in photosynthetic indicators,
To measure the diurnal variation in chlorophyll fluorescence, Fv/Fm, Y(II), Y(NPQ), Y(NO), and Fo, and Fm were measured using a portable chlorophyll fluorescence measurement device at 3-hour intervals (i.e., five times a day from 06:00–18:00 hour) in June and August 2022.
A certain area of the leaves of the collected target plant was separated and extracted by immersion in 5 mL of dimethyl sulfoxide for 48 hours at 30°C. The extract was subjected to absorbance measurements using a UV/VIS Spectrophotometer (OPTIZEN 2120; Mecasys Co. Ltd., Daejeon, Korea) at wavelengths of 665 nm, 649 nm, and 480 nm. The absorbance measurements were calculated as follows (Wellburn 1994):
Ca = 12.47
Cb = 25.06
Ca+b = Ca + Cb
Ca/b = Ca / Cb
Carotenoid = (1,000
The corresponding leaves were collected and fresh weight (FW) of the collected leaves was measured, and then the leaves were dried at 70°C for 72 hours using a desiccator (Forced Convection Oven, JSOF-150; JS Research Inc., Gongju, Korea). Next, their dry weight (DW) was measured, and the leaf water contents (LWCs) was calculated using the following equation.
LWC (%) = [(FW – DW) / FW] × 100
Leaf extracts were prepared by grinding dried plant leaves into a homogeneous powder using a grinder (Polymix Laboratory Dry Mill Drive Unit, PolymixTM PX-MFC 90 D; Kinematica AG, Luzern, Switzerland), and then placing taking a constant weight aliquot and placing it in a 25 mL measuring flask in a 90°C water bath for 1 hour. After allowing to cool at room temperature for sufficient time, the final volume was adjusted to 25 mL and extracted by filtering through a 0.45
T-test was performed using SPSS 26.0 (IBM Co., Armonk, NY, USA) to determine whether there were a significant differences between the measurements (
To investigate the changes in physiological characteristics of
The difference in wind speed between the two areas is related to geographical characteristics, as the coastal dunes of Goraebul, adjacent to the sea, are known to have higher average and instantaneous peak wind speeds and more frequent gusts compared to Kyungpook National University (Figs. 1C and 2C).
Soil moisture content also appears to be influenced by the time of measurement (Fig. 3C), and July and August, which recorded high soil moisture content, were periods of intensive precipitation during the study period, suggesting that the high soil moisture content measurements during these months were due to precipitation (Figs. 1C, 2C, and 3C). There was no significant seasonal difference in soil moisture content between the large pots at Kyungpook National University and the coastal dunes at Goraebull, where moisture was continuously supplied. This is likely due to the mulching effect of the undecomposed pine needles in the windbreak forest at the far end of the coastal dune where the plant grows, which suppresses the evaporation of soil moisture. Therefore, neither site appears to have been affected by severe water stress.
The VPDL, which is known to be influenced by temperature and relative humidity, was highest in June at both sites, but was 29.5% higher at Kyungpook National University than at Goraebul coastal sand dunes (Fig. 3D), indicating that the atmosphere was drier at Kyungpook National University. PAR, a measure of photon density in the wavelength bands available to plants for photosynthesis, was lower at Kyungpook National University than at Goraebul coastal sand dunes for most of the study period, which is likely due to frequent sun flecking by the pine tree crowns (Fig. 3A).
Seasonal changes in environmental factors affect the photosynthetic metrics of lichens, and these effects are shown in Fig. 4. The net photosynthetic rate (
In addition, photosynthetic indicators such as CE and stomatal conductance (
Water use efficiency can determine how much carbon a plant gains through photosynthesis while losing water through transpiration, and is known to be directly linked to physiological processes that regulate the gradient of CO2 and H2O at the leaf level (Hatfield and Dold 2019; Stanhill 1986). Large pot
We investigated the seasonal response of chlorophyll fluorescence, which can identify the activity of photosynthetic machinery, and found differences in chlorophyll fluorescence indicators among the study areas (Fig. 5). Light is the driving force of PSII, but it interferes with electron transfer, damages reaction centers including protein D1 in PSII, and causes photoinhibition, which inhibits the entire photosynthetic process (Aro et al. 1993a; Aro et al. 1993b). The proportion of Y(II) that processes the energy of photons in PSII was relatively low in most seasons in
In general, when plants are exposed to high PAR, they release excess photon energy in the form of heat through the NPQ mechanism to avoid photodamage, and a relatively small proportion is used for photosynthesis (Chen et al. 2016).
The Fv/Fm ratio is referred to as the maximum quantum yield and is an important indicator of the physiological state of a plant, which can be used to diagnose whether stress is occurring (Parkhill et al. 2001; Sharma et al. 2015). The Fv/Fm ratio measurements showed that compared to the coastal dunes, the
To understand the physiological response of
The photosynthetic characteristics of the diurnal variation showed different patterns depending on the time of measurement (Fig. 7). The June net photosynthetic rate (
In August, the WUE of the two sites showed the highest value at 12:00 hour and then decreased, which was related to the change in CE (Fig. 7E and 7F). This is believed to be a result of the inability to assimilate carbon effectively even with sufficient moisture supply, as the increase in leaf temperature under high temperatures leads to stomatal closure in addition to an increase in transpiration (
Y(II), an indicator of using the energy of photons for photochemical reactions, showed the lowest rate at 12:00 hour and the lowest Y(II) in June when the leaf temperature was the highest (Fig. 8).
The Y(II) value at 15:00 hour, when the temperature remained as high as 12:00 hour, recovered to the level at 09:00 hour. It is known that a combination of environmental factors such as high leaf temperature and PAR induce reversible inactivation of PSII. The recovery of Y(II) values suggests that
Various mechanisms, including the NPQ mechanism, are utilized to protect PSII from degradation, and differences in photoprotective mechanisms are known to occur depending on the time of year of measurement (Long et al. 1994). June measurements of Y(NPQ), which represents the proportion of NPQ mechanisms, decreased by 27.3% from 12:00 hour to 15:00 hour, whereas August measurements of large pots increased by 54.6% from 12:00 hour to 15:00 hour and August measurements of coastal dunes increased by 70% from 12:00 hour to 15:00 hour (Fig. 8). High foliar temperatures in June may inhibit the activity of the NPQ mechanism, and other mechanisms are utilized to prevent photoinhibition, including increased production of D1 protein, increased activity of photosynthetic enzymes used for carbon fixation, and activation of ROS scavenging systems (Aro et al. 1993b; Demmig-Adams and Adams 1992; Jahnke et al. 1991).
As a result, the Fv/Fm ratio, which indicates the physiological state of the plant, had the lowest value at 15:00 hour in
Chlorophyll plays a pivotal role in the photosynthesis process by transferring the energy of photons to the reaction center of PSII (Taiz and Zeiger 2010). In general, chlorophyll content can reflect the amount of photon energy absorbed per unit area and is a well-known indicator of physiological characteristics such as plant productivity (Anderson 1967; Zhang et al. 2021). Measurements of chlorophyll content over the season showed that
In general, environments with continuous cycles of strong and weak light, such as sun fleck, can induce inhibition of PSII as much as exposure to continuous strong light (Adams et al. 1999). The NPQ mechanism, the primary photoprotective response to PSII degradation, requires carotenoids such as violaxanthin, zeaxanthin, and antheraxanthin, which are utilized in the xanthophyll cycle (Gilmore 1997). The relatively high carotenoid content in the Goraebul coastal dune environment appears to be a mechanism for photoprotection of
Leaf water content, leaf osmolarity, TIC, and soluble carbohydrate content in June, when temperatures were at their highest, are shown in Table 1.
When summarizing the results of the meteorological and environmental factors of the two regions, the biggest difference between the two regions is temperature and sunlight, with Kyungpook National University’s environment having a high temperature and strong light, while Goraebul coastal sand dunes has a relatively low sunlight and low temperature.
Water use efficiency of
The decrease in Y(NPQ), the ratio of the NPQ mechanism, which is known to be one of the photoprotective mechanisms, is not only due to inhibition by strong light, but also to inhibition of the entire photosynthetic process. In order for the NPQ mechanism to operate, a ΔpH gradient must be established through the low pH of the thylakoid lumen (Ruban 2016; Tyystjärvi 2013). For this to occur, an adequate amount of ATP must be available. However, due to the high leaf temperature, the stomatal conductance (
In plants, ions, like soluble sugars, contribute to osmotic regulation and play a variety of roles, including redox reactions, energy storage, and carbon compound organization (Flowers and Yeo 1986; Taiz and Zeiger 2010). Thus,
In order to analyze the physiological and ecological characteristics of
The results of the photochemical characterization of
The coastal dune
Based on the analysis of the photochemical characteristics of
All the authors are deeply grateful to plant ecophysiology lab in Kyungpook National University, Republic of Korea.
LWC: Leaf water content
PAR: Photosynthetically active radiation
Y(II): The quantum yield of photochemical energy conversion in PSII
Y(NO): The quantum yield of non-regulated, non-photochemical energy loss in PSII
Y(NPQ): The quantum yield of regulated non-photochemical energy loss in PSII
ROS: Reactive oxygen species
LHC: Light harvest complex
NPQ: Non-photochemical quenching
VPDL: Vapor pressure deficit based on leaf
WUE: Water use efficiency
CE: Carboxylation efficiency
FW: Fresh weight
DW: Dry weight
YBK did data curation, investigation, and writing-original draft. SHY did data curation, funding acquisition, writing-review and editing. YSS did data analysis, writing-review and editing. YSC did conceptualization, supervision, writing-original draft, and writing-review and editing. All the authors approved the manuscript.
This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2016R1A6A1A05011910 & 2016R1D1A1B03934927), and by grants from the National Institute of Ecology (NIE-A-2023-20 & NIE-B-2023-02).
The data sets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.
The authors declare that they have no competing interests.
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Byoung-Jun Kim1†, Sung-Hwan Yim1,2†, Young-Seok Sim1 and Yeon-Sik Choo1,2*
Nam-Ho Roh1#, Jongsun Kim2#, Jaejin Park2 and Daesik Park2*
Sookyung Shin1, Jung-Hyun Kim2, Duhee Kang1, Jin-Seok Kim2, Hong Gu Kang3, Hyun-Do Jang1, Jongsung Lee1, Jeong Eun Han1 and Hyun Kyung Oh1*