Differential of three fields grown Juniperus species summer drought and cold hardening

ABSTRACT

Background:

Understanding species’ reactions to environmental stressors (cold and drought) and characterizing drought tolerance can help us understand their ecosystem responses related to global change. This study aimed to understand and compare the drought and cold tolerance strategies of Juniperus excelsa, Juniperus foetidissima, and Juniperus oxycedrus, which are found in the Western Mediterranean Region. Water relation parameters [ΨTLP (osmotic potential at turgor loss point), Ψ100 (osmotic potential at full turgor), Ɛmax (bulk modulus of elasticity), V0/DW (symplastic water at the saturated point per dry weight of the shoot), RWC (relative water content)] in summer and winter were determined. Total soluble sugar and photosynthetic pigment content were identified in spring, summer, autumn, and winter.

Results:

J. foetidissima had lower Ψ _TLP and higher Ɛmax in summer than other species. The species had similar Ψ _TLP ¹ Ψ ₁₀₀ ¹ Ɛmax, V0/DW, and RWC in winter. A seasonal change was observed in total soluble sugar and photosynthetic pigment content. Total soluble sugar and photosynthetic pigment contents were related to mean air temperature and total precipitation.

Conclusion:

J. foetidissima was more tolerant to water deficit in the summer, whereas the three species reacted similarly to the cold in the winter.

Keywords:
Drought; water status; cold resistance; soluble sugar; Juniperus; Mediterranean

HIGHLIGHTS

The water relations of Juniperus species were generally different in summer but similar in winter.

All three Juniperus species had lower total soluble sugar content in summer than in winter.

While photosynthetic pigment content was high in all three species in summer, it decreased in winter.

J. foetidissima was more tolerant to water deficit in summer than J. excelsa and J. oxycedrus.

INTRODUCTION

Arid and semi-arid regions constitute about 30% of the world's land surfaces ( Sène, 2004). Cold and drought are critical environmental stressors that affect plants' growth, productivity, and worldwide distribution ( Levitt, 1980). There is a large body of research on how species react to cold and drought ( Kubiske and Abrams, 1991; Ouyang et al., 2019). In general, plant production in the Mediterranean climate is limited by low temperatures and low radiation in winter and high water stress and high temperatures in summer ( Oliveria et al., 1992). Plants in regions with a Mediterranean climate have to cope with both long summer drought and short-term water stress due to high air temperature and evaporation ( Correia et al., 2001). When plants are gradually exposed to adverse growing conditions and environmental stressors, they make physiological and biochemical adjustments to prevent damage ( Scholz et al., 2012). At temperatures below freezing point, plants can survive either by avoiding or tolerating freezing ( Levitt, 1980). Trees use similar strategies (including avoidance and tolerance) to deal with stress ( Charrier et al., 2015). While the energy required for biochemical events increases, photosynthesis, carbohydrate transport, and respiration rates decrease at low temperatures ( Lambers et al., 2008). While water stress causes a reduction in osmotic potential at turgor loss point and osmotic potential at full turgor, it leads to an increase in the modulus of elasticity ( Pita and Pardos, 2001), and a change in photosynthetic pigment content ( Michelozzi et al., 1995). Ψ _TLP indicates the irreversible level of cell water losses and constitutes the limit where death or drying begins ( Genç and Yahyaoğlu, 2007). It is generally determined using pressure-volume (PV) curves ( Tyree and Richter 1982). Ɛ indicates how much turgor potential decreases during leaf water losses ( Saito et al., 2006). Elastic adaptation plays a critical role as a drought tolerance mechanism ( Bacelar et al., 2009). Characteristics related to plant-water relationships, such as Ψ _TLP Ψ ₁₀₀ and Ɛmax, are important parameters for assessing plants’ drought tolerance and adaptation ( Bartlett et al 2012; Zhu et al., 2018). Species with more negative water potential (i.e., turgor loss) are generally more drought tolerant ( Bartlett et al., 2016; Kunert 2020; Kunert et al., 2021).

Drought avoidance and tolerance determine the physiological effects of drought stress on a species and its distribution in habitats with varying soil water availability ( Parker et al., 1982). A plant's capacity to respond to stressors affects its geographic distribution. A significant part of the forest tree species in Türkiye is distributed in environments with summer drought and Mediterranean climatic conditions ( Dirik, 1994). Juniper species, known for their drought resistance, cover an area of 1 472 988 ha in Türkiye ( OGM, 2020). Due to their aesthetic body forms, junipers are ornamental trees (park and garden arrangements). They are also used in erosion control because they are resistant to extreme climate and soil conditions and have widespread root systems. They are valuable assets for the wood-based industry. They are also versatile wood species used in wind, snow, and sound curtains ( Gültekin et al., 2003). Juniperus excelsa Bieb. is found in stands in large areas in the forests of Türkiye. It stretches from marine climate zones to the steppe. It is resistant to heat, cold, and drought ( Eler, 2000). Durable and valuable wood is obtained from Juniperus foetidissima Willd. Juniperus oxycedrus L. can grow almost anywhere ( Anşin and Özkan, 2006). Juniperus species can adapt to extremely harsh environmental conditions (summer drought, winter frosts, shallow soil, etc.) that no other tree species can survive ( Douaihy et al., 2013). According to ecophysiological studies, different genotypes have different drought coping capacities, ( Villar et al., 2011) and different species have different levels of cold tolerance ( Charra-Vaskou et al., 2012). Climate change requires trees and forests to cope with new climatic and biotic conditions. Tree populations cope with new climatic conditions by either migrating or adapting. If they cannot cope, they vanish. We should understand the adaptation mechanisms of forests and trees to address their capacity to survive and thrive ( Chmura et al., 2011). This study had two objectives: (a) understanding and comparing the drought and cold tolerance strategies of J. foetidissima, J. excelsa and J. oxycedrus species under natural environmental conditions and (b) to determinining the seasonal changes in the osmotic potential at turgor loss point (Ψ _TLP), osmotic potential at full turgor (Ψ ₁₀₀), Ɛmax , symplastic water at a saturated point per dry weight of the shoot (V0/DW), relative water content (RWC), soluble sugar, and photosynthetic pigment content.

MATERIAL AND METHODS

Field sites and plants

The experimental plot is located Western Mediterranean Region in Türkiye (Isparta Regional Directorate of Forestry, Sütçüler Forestry Management Directorate 37°38'43'' N, 31°00'20'' E; 1366 m). It has a slope of 30% in the southeast. The study was conducted between April 2016 and January 2017. According to the data received from the nearest meteorological station, the experimental plot had a total precipitation rate of 880 mm, an average air temperature of 13.7 °C, and average air humidity of 58.0% between 2016 and 2017 ( Table 1; Figure 1).

Figure 1.
Total rainfall and air temperature at the experimental plot during the study period (2016-2017 years)

The hottest months (average 25.0 °C) were July and August, and the coldest (average 1.2 °C) was January during the study period. The total precipitation was 36.2 mm in April, 7.6 mm in August, 0.2 mm in October, and 148.6 mm in January (Fig. 1). The experimental plot is semi-moist according to the Erinc method based on the long-term averages of climate data ( Table 1). J. excelsa had mean diameter at breast height (cm) and mean height (m), 35.7±0.9 and 12.0±0.6, respectively. J. foetidissima had an average breast height diameter (cm) of 36.8±0.8 and a height (m) of 12.9±0.5. J. oxycedrus had an average breast height diameter (cm) of 16.1±0.8 and a height (m) of 3.6±0.4. The experimental plot was 1 ha in size.

Table 1.
Monthly rainfall and air temperature at the experimental plot during 1961–1992, 2007-2017 and 2016-2017 for the year

	Months												Annual
	Jan.	Feb.	Mar.	Apr.	May	June	July	Aug.	Sep.	Oct.	Nov.	Dec.
Rainfall 1961-1992 (mm)	141.4	129.3	91.6	86.6	63.7	35.3	11.3	11.8	32.6	68.3	101.4	163.8	937.1
Rainfall 2007-2017 (mm)	146.9	110.1	90.5	55.5	73.3	39.5	6.0	11.6	36.9	94.1	82.5	140.8	887.6
Rainfall 2016-2017 (mm)	166.6	38.1	101.0	47.2	129.7	88.4	10.2	16.2	22.6	25.9	141.0	93.1	880.0
Temperature 1961-1992 (°C)	3.4	3.9	7.0	11.3	15.9	20.6	24.3	24.0	20.0	14.7	9.1	5.0	13.3
Temperature 2007-2017 (°C)	3.7	5.0	7.8	11.8	16.1	21.2	25.3	25.5	21.1	15.2	10.2	5.9	14.1
Temperature 2016-2017 (°C)	1.9	6.0	8.0	12.7	14.9	21.1	25.6	24.4	20.9	15.5	9.0	4.6	13.7

Pressure volume analyses

Water relation parameters were examined in the summer (August) and winter (January). Shoot samples were collected from the south side of the crown and the lower 2/3 of the ten sample trees from each species Shoots (15-20 cm) were collected from J. foetidissima, J. excelsa, and J. oxycedrus. Water potential components were detected on three randomly selected shoot samples. The shoots were immediately put in plastic bags and placed in a mini-fridge with ice sockets inside. They were then brought back to the laboratory. The Pressure-Volume (P-V) curve method was used to determine the water potential components. Measurements were made using a plant chamber device (PMS Instrument Co., Corvalis, OR, USA) ( Scholander et al., 1965). They were cleaned under water and dried. Then their fresh weights (FW) (at 0.001 g sensitivity) were determined. Afterward, they were placed in distilled water and kept in the dark at room temperature for 24 hours. Their saturation weights (SW) were identified. They were then immediately placed in a plant pressure chamber device. They were kept for 10 minutes with an increase in pressure steps of 0.3 MPa ( Ritchie, 1984) The measurement continued until the water potential became -4.0 or -4.5 MPa. Afterward, their end of measure weights were determined. They were then kept in a drying oven at 105 °C for 24 hours, and their oven-dried weight (DW) was then identified. Ψ _TLP, Ψ ₁₀₀, and symplastic water content are determined using pressure-volume curves, while RWC and Ɛmax are calculated using the following equations: ( Parker and Pallardy, 1988; Gross and Koch, 1991; Colombo and Teng 1992; Mitchell et al 2008; İmal, 2015).

\[ \begin{equation} RWC=\left[\left(FW-DW\right)/\left(SW-DW\right)\right]\ast100 \end{equation} \]

\[ \begin{equation} \varepsilon max=\left(\Psi_{P1}-\Psi_{P2}\right)/\left[\left(V_1-V_2\right)/V\right] \end{equation} \]

where Ψ _P1 and Ψ _P2 are turgor pressures determined at 3-5 % intervals of RWC, V ₁ and V ₂ are symplast water volume at Ψ _P1 and Ψ _P2, respectively. V is total symplast volume at full turgor.

Photosynthetic pigment and total soluble sugar

Ten shoots were collected from each species ( J. foetidissima, J. excelsa and J. oxycedrus) randomly selected in the experimental plot. Soluble sugar and photosynthetic pigment analyses were performed on the same trees using shoots collected for the P-V curve. Total soluble sugar and photosynthetic pigment content were determined in needles in the spring (April), summer (August), autumn (October), and winter (January). The chlorophyll pigment content was determined on fresh samples according to Arnon ( 1949). Measurements were made in a spectrophotometer at 450, 645, and 663 nm wavelengths. Total soluble sugar was determined on dry samples using the phenol sulfuric acid method ( Dubois et al., 1956).

Data analysis

The data were analyzed using the Statistical Package for Social Sciences (SPSS v. 25.0). A two-way analysis of variance was used to determine whether species, season, and speciesXseason affected Ψ _TLP, Ψ ₁₀₀, Ɛmax, V0/DW, RWC, soluble sugar, and photosynthetic pigment. Duncan's test was used to compare the means. The student's t-test was used to determine any significant difference in physiological and biochemical properties between summer and winter. Principal component analysis (PCA) was also used to determine the relationship between variables and physiological and biochemical properties.

RESULTS

Osmotic potential at turgor loss point depended is seasonal and species dependent, while the osmotic potential at full turgor is species dependent ( Table 2; P<0.05). J. excelsa showed higher osmotic potential at turgor loss point in summer than in winter. In summer, J. foetidissima showed lower osmotic potential at the turgor loss point and osmotic potential at full turgor than J. excelsa and J. oxycedrus. There was no significant difference in osmotic potential at full turgor between the species in winter ( Figure 2).

Table 2.
The statistical significance (P>F) of main effects of season, species and seasonxspecies interactions on Ψ _TLP, Ψ ₁₀₀, Ɛmax, V0/DW, RWC, TSS, Chla, Chlb and Chla+b.

Factors	Season	Species	Season x Species
Ψ TLP (MPa)	<0.01	<0.001	0.177
Ψ 100 (MPa)	0.889	<0.05	0.378
Ɛmax (MPa)	0.883	<0.01	0.443
V0/DW	0.335	0.496	0.632
RWC (%)	<0.001	<0.01	0.129
TSS (mg g -1 DW)	<0.001	<0.001	0.077
Chla (mg g -1)	<0.001	<0.001	<0.05
Chlb (mg g -1)	<0.001	0.588	0.129
Chla+b (mg g -1)	<0.001	<0.01	<0.05

Significant effects are highlighted in bold.

Season and species affected RWC and species affected Ɛmax ( Table 2; P <0.05). According to the pressure-volume (P-V) curve analysis, J. foetidissima showed highest Ɛmax in summer ( Fig. 3a). J. excelsa and J. foetidissima had higher RWC than J. oxycedrus in winter ( Fig. 3c).

Figure 2.
Changes in Ψ _TLP (osmotic potential at turgor loss point) and Ψ ₁₀₀ (osmotic potential at full turgor) in summer (2016 year) and winter (2017 year) seasons in Juniperus excelsa, Juniperus foetidissima and Juniperus oxycedrus (Means ± standard error; capital letters mean difference between in seasons; lower case letters mean the difference between species.

Figure 3.
Plant water relation parameters [a:Ɛmax (MPa), b:V0/DW, c:RWC (%)] in summer (2016 year) and winter (2017 year) seasons in Juniperus excelsa, Juniperus foetidissima and Juniperus oxycedrus (Means ± standard error; capital letters mean difference between in seasons; lower case letters mean the difference between species.

Season and species affected total soluble sugar, Chla, and Chla+b. The total soluble sugar content, which was high in spring, decreased in summer but increased again in autumn and winter in all species ( Fig. 4). All three species had the lowest soluble sugar content in summer. J. oxycedrus showed highest total soluble sugar content in summer and winter.

Figure 4.
Variation of total soluble sugar content according to seasons (2016-2017 years) in Juniperus excelsa, Juniperus foetidissima and Juniperus oxycedrus (Means ± standard error; capital letters mean difference between in seasons; lower case letters mean the difference between species.

Photosynthetic pigment content, which was generally low in spring, increased in summer and then decreased towards autumn and winter. J. oxycedrus showed highest and J.excelsa showed lowest Chla in the spring, autumn and winter. All three species had similar photosynthetic pigment content in summer ( Fig. 5a-b-c).

Figure 5.
Variation of photosynthetic pigment content (a:Chl a, b:Chl b and c:Chla+Chlb) according to seasons (2016-2017 years) in Juniperus excelsa, Juniperus foetidissima and Juniperus oxycedrus (Means ± standard error; capital letters mean difference between in seasons; lower case letters mean the difference between species.

According to the PCA analysis, RWC (r:0.854), TSS (r:0.621), Chla (r:-0.918), Chlb (r:-0.883), Total Chl (r:-0.933), mean air temperature (r:-0.921), and total precipitation (r:0.921) had the highest correlation with Axis 1 (52.8 %) ( Fig. 6). According to Axis 1, there was a correlation between air temperature and Chl a, Chl b, and total chlorophyll content, while there was a correlation between total precipitation and RWC and TSS. According to the PCA analysis, Ψ _TLP (r:-0.615), Ψ ₁₀₀ (r:-0.669) and Ɛmax (r:0.791) had the highest correlation with Axis 2 (25.5%). There was a correlation between osmotic potential at the turgor loss point, osmotic potential at full turgor and Emax.

Figure 6.
Figure 6. Principal component analysis (PCA) of Ψ _TLP, Ψ ₁₀₀, Ɛmax , V0/DW, RWC, TCC, Chla, Chl b and total Chl in J. foetidissima (Jf), J. excelsa (Je) and J. oxycedrus (Jo) (wint: winter, summ:summer)

DISCUSSION

Ψ _TLP measurements showed that J. excelsa and J. oxycedrus reach their Ψ _TLP earlier than J. foetidissima under water limitations in summer, while all three species had similar Ψ _TLP in winter. Research shows a reduction in Ψ _TLP in response to cold and drought depending on the species ( Anisko and Lindstrom, 1996; White et al., 1996; Maréchaux et al., 2015). J. foetidissima had the lowest Ψ _TLP in the summer and improved drought tolerance compared to the other two species. The species with the least negative osmotic potential at turgor loss point is least adapted to drought ( Duhme and Hinckley, 1992). Plants with more negative Ψ _TLP can resist leaf dehydration and thus maintain stomatal conductance, photosynthesis, and growth under lower water availability ( Tognetti et al., 2000). J. foetidissima showed highest Ɛmax in summer. The lower Ψ _TLP and Ψ ₁₀₀, the higher Ɛmax (i.e.the lowest tissue elasticity). In summer, J. foetidissima showed high Ɛmax, retaining more symplastic water within its cells during the reduction of turgor potential. Cells with a high elastic modulus retain more water than other cells at or near Ψ _TLP ( Colombo, 1987). With low cell wall elasticity, J. foetidissima showed higher tolerance and adaptation than other Juniperus species in water deficit. Plants with high Ɛmax are more drought tolerant ( Ritchie and Schula, 1984). Ψ _TLP varies from season to season ( Mitchell et al., 2008; Deligöz et al., 2021). Differences in physiological responses to water deficiency show that alternative mechanisms (osmotic or elastic adjustment) are important for leaf tissue integrity and survival ( Mitchell et al., 2008). The osmotic and elastic adaptability of woody plants varies from species to species ( Sanders and Arndt, 2012). It is related to plant phenology ( Kubiske and Abrams, 1991) and is largely dependent on environmental conditions ( Leuschner et al., 2019). In the present study, mean air temperature and total precipitation were related to total soluble sugar and photosynthetic pigment contents. J. excelsa had lower Ψ _TLP but a higher total soluble sugar content in the winter than in the summer. In general, the low osmotic potential in winter may be related to an increase in the number of osmolytes dissolved in leaf cells. In addition, this decrease may be a cold hardening reaction ( Harayama et al., 2006). Ritchie and Schula ( 1984) reported that the decrease in the osmotic potential at the turgor loss point and full turgor in Pseudotsuga menzeisii (Mirb.) might be due to sugar accumulation. On the other hand, Gross and Koch ( 1991) stated that the decrease in the osmotic potential at the turgor loss point and full turgor in Picea abies L. might be due to the change in symplastic volume rather than the change in soluble content. All three species had similar V0/DW in the summer and winter. In general, symplastic water at a saturated point per dry weight of the shoot is high in spring but decreases in summer and winter ( Tognetti et al., 2000). Relative water content is a sensitive variable that responds rapidly to environmental conditions (temperature, light, humidity, and water supply) ( Tanentzap, 2015) and directly reflects the water status of plants ( Yang and Miao, 2010). Compare to the species, J. excelsa and J. foetidissima showed higher RWC than Juniperus oxycedrus in winter. A relative water content of 40 to 60% results in desiccation damage ( Vostral et al., 2002). None of the species had an RWC of lower than 86%. High leaf water content converts excess energy into heat and reduces damage to chloroplasts ( Tomlinson et al., 2013).

Total precipitation was correlated with RWC and TSS. Generally, non-structural carbohydrates are high in winter, decrease in summer, and increase again ( Diamantoglou et al., 1989; Palacio et al., 2018). During cold months, soluble sugar content increases as starch concentrations decrease. This sugar may play a role in cold tolerance ( Wong et al., 2003). In the summer and winter, J. oxycedrus had higher total soluble sugar content than J. excelsa and J. foetidissima. However, all three species had similar total soluble sugar content in the autumn. High sugar content in autumn may make plants more resistant to cold ( Schaberg et al., 2000). In autumn and winter, soluble carbohydrates cause an increase in leaf concentration, which has been associated with frost hardening ( Oleksyn et al., 2000). The number of frost days in the experimental plot was 22 in January. Soluble sugar content increased in the autumn and winter compared to the summer. This may also be related to cold tolerance. Woody plants can adapt to temperatures below freezing point to survive cold stress. First, they get used to it partially in short days. Later, low temperatures and prolonged subfreezing temperatures trigger the plant, resulting in midwinter cold hardiness ( Weiser, 1970). Trees also need to store reserves to survive winter and burst buds and grow shoots the following spring ( Regier et al., 2010). Seasonal changes in carbohydrate concentration can be largely explained by leaf phenology ( Neweel et al., 2002). Photosynthetic pigment content is another parameter that changes seasonally. Photosynthetic pigment content, which was generally low in the spring and winter, was high in the summer. Plants adjust chlorophyll content to adapt to environmental conditions ( Bayar and Deligöz, 2021). Photosynthetic pigments usually increase at the end of the growing season. The high level of chlorophyll pigments late in the season (august) is an adaptive protective mechanism in stressed plants ( Kulaç et al., 2012). There was a positive correlation between annual mean maximum temperature and photosynthetic pigment content ( Yücedağ et al., 2021). All three species had higher Chla, Chlb, and Chla+b with an increase in average air temperature. Season affected photosynthetic pigment content ( Wolkerstorfer et al., 2011; Bündchen et al., 2016). Seasonal changes in photosynthetic pigment content (Chla+b) are controlled by the daily light period. The best frost-resistant needles contain fewer photosynthetic units ( Vogg et al., 1998). There is a consistent relationship between photosynthetic pigment content and light ( Minotta and Pinzauti 1996) and temperature affects photosynthetic pigment content ( Ottander et al., 1995). J. excelsa showed lowest Chla in the winter. Photosynthetic pigment content varies by year, season, and species ( Uvalle Sauceda et al., 2008).

CONCLUSIONS

Ecophysiological processes are the basis of evolutionary adaptation to climate change ( Chmura et al., 2011). Reductions in elasticity (high Ɛmax) were associated with drought tolerance. Juniperus species had different elastic responses to drought. Results showed that J. foetidissima is more drought tolerant and adapted to summer water deficit better than J. excelsa and J. oxycedrus. Ψ _TLP provides important information about a species' capacity to tolerate drought conditions and can be used to select drought-tolerant species. The cold tolerance of the species (similar Ψ _TLP, Ψ ₁₀₀, and Ɛmax) in winter was also similar. We should make more measurements detailing the selection criteria for cold resistance and conduct more research on the role of water relations parameters ( _TLP, Ψ ₁₀₀, and Ɛmax) and soluble carbohydrate content in osmotic regulation in seasonal variation.

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Data availability

Data citations

OGM (FOREST GENERAL DIRECTORATE). Ormancılık İstatistikleri 2020. Available et: https://www.ogm.gov.tr/tr/e-kutuphane/resmi-istatistikler Accessed in:April 10th 2021.

Publication Dates

• Publication in this collection
  16 Dec 2022
• Date of issue
  2022

History

• Received
  28 Apr 2022
• Accepted
  23 June 2022