Research ArticleArticles

Changes in Leaf Thickness, Chlorophyll Content, and Gas Exchange of a Landscape Tree, Xanthostemon chrysanthus, Treated with Paclobutrazol and Potassium Nitrate

Ahmad Nazarudin Mohd Roseli, Tsan Fui Ying and Normaniza Osman
Arboriculture & Urban Forestry (AUF) March 2021, 47 (2) 53-63; DOI: https://doi.org/10.48044/jauf.2021.005

Abstract

Paclobutrazol (PBZ)(0 g L−1, 0.125 g L−1, and 0.25 g L−1) and potassium nitrate (KNO3)(0 g tree−1, 100 g tree−1, and 200 g tree−1) were tested on a landscape tree, Xanthostemon chrysanthus (F. Muell.) Benth., in an attempt to enhance its stress tolerance under harsh urban conditions. Significant effects on tree height, diameter at breast height, canopy diameter, leaf area, and anatomy of tree leaves and stems in response to PBZ and KNO3 have been previously reported; in addition to these, the influences on leaf thickness and leaf physiology, including chlorophyll content and gas exchange, are discussed in this study. Relative chlorophyll content was significantly increased with PBZ and/or KNO3, enhancing leaf greenness. Increased leaf thickness of up to 13.37% at 6 months after treatment with a combination of PBZ and KNO3 was observed. The presence of PBZ significantly reduced the photosynthetic and transpiration rates and stomatal conductance. Reduced leaf physiological traits combined with thicker leaves would be beneficial for trees to tolerate harsh urban settings. Therefore, a combination of PBZ and KNO3 is recommended for stress tolerance enhancement of X. chrysanthus grown as a landscape tree.

Keywords

INTRODUCTION

A triazole compound, paclobutrazol, PBZ [(2RS, 3RS)-1-(4-chlorophenyl)-4,4-dimethyl-2-(1H-1,2,4-triazol-1-yl) pentan-3-ol] is widely used in managing ornamental plants. It is an inhibitor of ent-kaurenoic oxidase, a key enzyme in the gibberellin (GA) biosynthesis pathway. Application of PBZ reduces GA content in plants, reducing cell elongation and inhibiting growth. As an anti-GA compound, PBZ has been shown to control growth of several plant species (Mohammed et al. 2016; Xia et al. 2018; Ju et al. 2019). Obvious plant responses to PBZ treatment were reduced growth of new shoots, stem diameter, and leaf area; enhanced chlorophyll content; and modified flowering and phytochemical contents in plants (Ahmad Nazarudin et al. 2007; Ahmad Nazarudin 2012; García De Niz et al. 2014). PBZ increased the size of vascular bundles, chloroplasts, and epidermal, mesophyll, and bundle sheath cells in nonwoody plants (Burrows et al. 1992; Gopi et al. 2008; Gao et al. 2011). Only a few studies reported the effects of PBZ on the anatomy of woody plants, including Syzygium campanulatum (Ahmad Nazarudin et al. 2007) and Toona ciliata (Rodrigues et al. 2016). Plants treated with PBZ were also physiologically affected. In potted Syzygium myrtifolium, PBZ reduced both photosynthetic and transpiration rates, though the stomatal conductance was not significantly affected (Ahmad Nazarudin et al. 2012). However, in T. ciliata, the gas exchange parameters remained unaffected with PBZ application (Rodrigues et al. 2016). This heterocyclic compound also increases plants’ tolerance towards abiotic stresses—for example, drought, flooding, chilling, and salinity. Several other studies reported that PBZ was able to improve water stress tolerance in woody plants such as Phillyrea angustifolia (Fernandez et al. 2006) and Mangifera indica (Kishor et al. 2009).

Apart from use of PBZ, correcting issues with culture and remedying nutrient and other deficiencies will typically increase tree growth. However, the application of suitable treatments on landscape trees can be overlooked, hence causing a decline in the growth performance of the trees. For instance, potassium is an essential nutrient and is required for desirable growth of plants. It is essential for the activation of over 80 enzymes throughout the plant (Mengel 2007), improving the plant’s ability to withstand extreme conditions such as cold and heat, prolonged drought, and pest and disease attacks (Umar 2006; Thomas and Thomas 2009). Trees planted in urban areas are easily exposed to these growth challenges and need additional attention to ensure their survival.

Although proper application of PBZ and potassium could enhance abiotic stress tolerance in urban trees, studies of managing such trees under local climatic conditions have not been carried out extensively. Thus, Xanthostemon chrysanthus (F. Muell.) Benth. (Myrtaceae), commonly known as golden penda, was selected as a model tree for this study. This species is native to tropical northern Australia, New Caledonia, New Guinea, Indonesia, and the Philippines (Sosef et al. 1998). It has also been widely domesticated in Malaysian cities. It is a medium-sized tree that reaches 10 to 15 m in height in its natural habitat. It has bright yellow compound flowers 8 to 12 cm in diameter. Due to its distinctive flowers and dense tree crown, this is a locally preferred species for beautifying residential areas, parks, and roadsides.

This study aimed to determine the effects of PBZ and potassium nitrate (KNO3) on leaf attributes such as leaf thickness, relative chlorophyll content, and gas exchange in X. chrysanthus. Our previous investigation found significant reduction of tree growth in terms of plant height, diameter at breast height, crown diameter, and leaf area of the species in the presence of PBZ (Ahmad Nazarudin et al. 2015). We also observed that the palisade parenchyma thickness was greatly increased after treatment with 0.25 PBZ g L−1 + 200 g KNO3 (Ahmad Nazarudin et al. 2015). However, spongy parenchyma thickness was unaffected by the treatments. Thus, it is also essential to explore the effects of these treatments on leaf thickness and leaf physiology, including chlorophyll content and gas exchange. These assessments were important in order to evaluate the potential of PBZ and KNO3 to enhance stress tolerance without causing detrimental effects to morphological and physiological traits of the species.

MATERIALS AND METHODS

Study Site and Plant Materials

A total of 81 existing X. chrysanthus trees grown at Metropolitan Batu Park, Kuala Lumpur (3°12′49″N, 101°40′43″E) were selected randomly for this study (Figure 1). The trees were planted and maintained by the Kuala Lumpur City Hall (KLCH). For the purposes of the experiment, all trees were selected based on their good growth performance in terms of leaf area index and for being free from pests and diseases. These trees had leaf area index values ranging from 2 to 2.41, heights from 6.01 to 6.91 m, and trunk diameters from 11.02 to 13.70 cm. The trees were planted 1 to 1.5 m away from the road shoulder and 10 m from one another. Nine treatment combinations of PBZ and KNO3 (control, 100 g KNO3, 200 g KNO3, 0.125 g L−1 PBZ, 0.125 g L−1 PBZ + 100 g KNO3, 0.125 g L−1 PBZ + 200 g KNO3, 0.25 g L−1 PBZ, 0.25 g L−1 PBZ + 100 g KNO3, and 0.25 g L−1 PBZ + 200 g KNO3) with nine replications were laid out in a completely randomized design. No PBZ or KNO3 was applied to the control trees.

Figure 1.
Figure 1.

Xanthostemon chrysanthus planted by the roadside of Metropolitan Batu Park.

Cultar®, containing 250 g a.i. PBZ L−1, and Krista™ K Plus (13.7:0:46.3) as the source of KNO3 were used in this study. PBZ was diluted with water prior to application into soil around the root collar of the trees. Each tree received 1 L of PBZ dilution, while the control tree received 1 L of tap water. PBZ was applied once at the beginning of the study (March 2012). On the other hand, each dosage of granular KNO3 was applied at 3-month intervals. The first application of KNO3 was done concurrently with PBZ treatment. KNO3 was applied directly into the soil because the KLCH did not allow foliar spraying for trees grown in the park. Thus, pocket application of KNO3 was carried out under the tree-canopy drip line to avoid surface runoff during rainy days. Each dosage of KNO3 was equally divided into 4 portions, each of which was placed approximately equidistant from the others around the canopy drip line. The study was carried out for a year, from March 2012 to March 2013. During the study period, total precipitation received was 3,181.7 mm while the average temperature was between 22.9 and 33.3 °C with relative humidity of 76.4%.

Measurement of Leaf Relative Chlorophyll Content

For the relative chlorophyll content (leaf greenness) investigation, in situ measurement was performed by using a portable chlorophyll meter (SPAD-502, Minolta, Japan). The first fully expanded leaves from 3 branches of each tree were selected randomly for the measurement. Relative chlorophyll content was recorded monthly from April 2012 to March 2013 after PBZ and initial KNO3 treatment. A total of 27 leaves per treatment were measured in monthly sampling.

Determination of Leaf Thickness Increase

Changes in leaf thickness (μm) of X. chrysanthus were assessed before treatment (March 2012) and at 6 months after treatment with PBZ and KNO3 (September 2012). The first fully expanded leaves from 5 randomly selected vegetative branches of each tree were collected for the assessment. Leaf specimens were prepared and observed under a scanning electron microscope (JEOL JSM-5610LV) as described in Ahmad Nazarudin et al. (2015). The thickness increase (%) of the palisade, spongy parenchyma, and leaf was then determined. A total of 45 leaves per treatment were sampled for the assessment.

Measurement of Leaf Gas Exchange

The youngest fully expanded leaves from 3 vegetative branches were selected randomly from each tree for measurement of leaf gas exchange. The measurement was conducted using a portable infrared gas exchange analyzer (Li-6400XT, LICOR, Nebraska, USA). Measurements of photosynthetic rate (μmol m−2 s−1), transpiration rate (mmol m−2 s−1), and stomatal conductance (mol m−2 s−1) were performed between 9:00 a.m. and 11:00 a.m. when photosynthetically active radiation was in the range of 500 to 1200 μmol m−2 s−1 and carbon dioxide concentration was at 360 to 400 ppm. The measurement was made at ambient humidity and at a maintained temperature of 28 °C. A total of 27 leaves per treatment were measured in each observation. The first and second observations were made in September 2012 and March 2013, respectively.

Statistical Analysis

All data were subjected to 2-way analysis of variance (ANOVA) using Statistical Analysis System version 8.1 (SAS Institute Inc., Cary, NC, USA). Differences between treatment means were compared by using Duncan’s multiple range test (DMRT) at 5% level of probability.

RESULTS

Leaf Relative Chlorophyll Content

Initial measurements in April 2012 showed that the leaf relative chlorophyll content was statistically equal among treatments (Table 1). In May 2012, 2 months after treatment, differences in this leaf attribute began to be found. At this stage, the relative chlorophyll content in the control trees was significantly lower than in other treatments. At 6 months after treatment, a difference of about 20% was exhibited between the highest relative chlorophyll content in 0.125 g L−1 PBZ + 100 g KNO3-treated trees and the lowest value in the control trees. However, no significant differences in this leaf attribute were observed among trees treated with PBZ or KNO3 alone or in combination. These results showed that the relative chlorophyll content in the leaves was markedly augmented with the presence of PBZ and KNO3, increasing the leaf greenness (Figure 2). This trend of changes in relative chlorophyll content was continuously observed throughout the study period.

View this table:
Table 1.

Monthly changes in relative chlorophyll content of X. chrysanthus treated with PBZ and KNO3.

Figure 2.
Figure 2.

Comparison of leaf size and greenness in X. chrysanthus at 6 months after treatment with PBZ and KNO3.

Leaf Thickness Increase

Observations via scanning electron microscope discovered that X. chrysanthus leaves have one layer of palisade parenchyma, and the spongy parenchyma has a few intercellular spaces (Figure 3). Application of PBZ modified the arrangement of mesophyll cells, making the leaf more compacted (Figure 3c and 3d) as compared to those of the untreated controls (Figure 3a) and KNO3-treated leaves (Figure 3b). Observation at 6 months after treatment with 0.25 g L−1 PBZ + 200 g KNO3 showed an increase of palisade parenchyma thickness of up to 51.12%, while the controls only showed a 2.49% thickness increase over measurements recorded at the start of the study (Table 2). It has been proven in our previous investigation that trees treated with the combination of PBZ and KNO3 resulted in greater values of palisade parenchyma thickness as compared to those treated with PBZ or KNO3 alone (Ahmad Nazarudin et al. 2015). At the same time, treatments with KNO3 alone (100 g KNO3 and 200 g KNO3) have a thicker palisade parenchyma as compared to the control trees at 6 months after treatment (Ahmad Nazarudin et al. 2015). As a consequence of the increased palisade parenchyma layer thickness, the leaf thickness of X. chrysanthus also increased (Table 3). In this study, the leaf thickness increase in the trees treated with 0.25 g L−1 PBZ + 200 g KNO3 was 13.37%, while there was only a 0.91% increase for this parameter among the controls (Table 3). Application of PBZ or KNO3 alone increased the leaf thickness by approximately 10% and 4.9%, respectively.

Figure 3.
Figure 3.

Micrographs of X. chrysanthus leaves at 6 months after treatment with PBZ and KNO3. (a) Untreated control leaf; (b) KNO3-treated leaf; (c) PBZ-treated leaf; (d) PBZ + KNO3-treated leaf. Palisade parenchyma (P); Spongy parenchyma (S); Epidermis (E); Cuticle (C).

View this table:
Table 2.

Thickness increase of palisade and spongy parenchyma in X. chrysanthus at 6 months after treatment with PBZ and KNO3.

View this table:
Table 3.

Changes in leaf thickness of X. chrysanthus at 6 months after treatment with PBZ and KNO3.

Leaf Physiological Performance

Photosynthesis, transpiration, and stomatal conductance were significantly different among treatments at 6 and 12 months after the treatment (Table 4). The highest photosynthetic rate was found in the control trees. This study showed equal response in photosynthetic rate between trees treated with different amounts of PBZ alone, and between trees treated with different amounts of KNO3 alone. There was also a statistically equal photosynthetic rate among trees that had combined treatments of PBZ and KNO3. However, comparison among different treatments revealed that the presence of PBZ resulted in lower rates of photosynthesis than in trees treated with KNO3 alone and the control trees. At 6 months after treatment, the highest photosynthetic rate was 6.56 μmol m−2s−1 in the control trees, while trees treated with 0.25 g L−1 PBZ had the lowest photosynthetic rate (3.25 μmol m−2s−1), almost a twofold difference. At this stage, the highest transpiration rate was recorded in the control trees, while the lowest was demonstrated by 0.25 g L−1 PBZ + 200 g KNO3-treated trees (Table 4). The transpiration rate of the control trees was higher by 75.33% than those trees treated with 0.25 g L−1 PBZ + 200 g KNO3. Comparison between different rates of PBZ or KNO3 tested alone, and among combined treatments of both compounds gave no differences in terms of transpiration rate. This study suggested that the transpiration rate of the trees markedly decreased in the presence of PBZ. As for stomatal conductance, no significant differences were demonstrated between the two treatment levels of PBZ alone or the two levels of KNO3 alone. Nor were significant differences shown among trees treated with combined treatments of PBZ and KNO3. However, the presence of PBZ triazole significantly reduced the stomatal conductance, resulting in lower values as compared to those of the KNO3-treated trees and the controls (Table 4). These treatments showed similar responses in photosynthetic rates, transpiration rates, and stomatal conductance at 12 months after treatment as they did at 6 months.

View this table:
Table 4.

Physiological response of X. chrysanthus at 6 and 12 months after treatment with PBZ and KNO3.

DISCUSSION

Urban trees are exposed to unfavorable biotic and abiotic stresses such as hot and cold temperatures, drought, poor soil conditions, and pests and diseases. These factors, which can lead to a decline in growth performance, are among the challenges facing trees in urban areas. Thus, maintenance approaches that enhance growth of urban trees are indeed essential. This study explored one possible technique for mitigating urban stresses in an existing landscape tree, X. chrysanthus, by looking into the possibility of using PBZ and KNO3 to improve the tree’s tolerance towards those challenges.

Our previous study indicated that the presence of PBZ suppressed leaf expansion, producing smaller leaf area as compared to those of other treatments (Ahmad Nazarudin et al. 2015). However, no abnormal leaf formation (leaf discoloration or anomalous growth) was observed (Figure 2), showing that the dosages of PBZ used in this study were appropriate for the species. The reduced size of PBZ-treated leaves may be associated to PBZ’s inhibitory action on GA biosynthesis, which is involved in cell elongation (Ahmad Nazarudin et al. 2015). Several other studies also showed reduced leaf area following PBZ treatment (Yeshitela et al. 2004; Chorbadjian et al. 2011; Ahmad Nazarudin et al. 2012). In addition, a darker green color in leaves was exhibited as a response to PBZ and KNO3 treatments (Figure 2). This was due to enhanced relative chlorophyll content associated with smaller leaf area, which further intensified the foliage color. Increased relative chlorophyll content as a response to PBZ was consistently reported in various plant species including Hibiscus rosa-sinensis (Ahmad Nazarudin 2012), Lagerstroemia indica (Mohammed et al. 2016), and Paeonia lactiflora (Xia et al. 2018).

Furthermore, the combination of PBZ and KNO3 produced relatively thicker leaves as compared to those treated with either PBZ or KNO3 alone. This study corroborates findings by Gopi et al. (2008) and Gao et al. (2011) which indicated that PBZ increased the leaf thickness of Amorphophallus campanulatus and Triticum aestivum, respectively. Increased leaf thickness also resulted from inhibition of leaf size in combination with further thickening of the palisade mesophyll cells. An enhanced palisade layer in other woody species such as S. campanulatum (Ahmad Nazarudin et al. 2007) and T. ciliata (Rodrigues et al. 2016) following PBZ application has also been documented. A previous study has also shown that PBZ resulted in thicker leaves in Chrysanthemum due to an additional layer of palisade, although individual palisade cells were shorter (Burrows et al. 1992). In the present study, observation through a scanning electron microscope proved that the X. chrysanthus leaf retained a single layer of palisade parenchyma. Therefore, the enhancement of leaf thickness in this species was actually influenced by the increased palisade parenchyma thickness rather than the additional layer of the palisade. Other than PBZ, potassium was also proven to increase chlorophyll content and leaf thickness in Gossypium hirsutum (Akhtar et al. 2009). Enhanced leaf thickness due to PBZ and KNO3 as observed in this study might be beneficial for X. chrysanthus to prevent biotic and abiotic stresses. Leaf thickness plays an essential role in plant functioning and relates to a species’ strategy for resource acquisition and use (Vile et al. 2005). Increased tissue thickness in the leaf enabling enhanced water-holding capacity with the presence of potassium helped improve metabolic activities and production of photosynthates like carbohydrates and proteins and their translocation to respective sinks. For example, Australian desert plants have relatively thick, long-lived leaves (Wright and Westoby 2002) and grow in soils that are uncommonly low in nutrients (Morton et al. 2011). Under such conditions, prolonging the leaf life span could be achieved through the production of leaves that are not only structurally tough and herbivore resistant, but also resistant to thermal damage (Leigh et al. 2012). In addition, physical modification of leaves as a response to PBZ, for example thicker leaves, smaller stomatal pores, and an expanded epicuticular wax layer on the leaf surface, may provide additional protections against various fungal, bacterial, and insect infestations (Chaney 2005).

In the present study, a significant reduction in photosynthetic rates, transpiration rates, and stomatal conductance was demonstrated in the presence of the PBZ compound. Similar results of reduced photosynthetic rate as a response to PBZ treatment were also reported in L. indica (Mohammed et al. 2016) and S. myrtifolium (Ahmad Nazarudin et al. 2012). This could be the indirect effect of modified cell arrangement in the leaves caused by PBZ, which eventually restricted gas exchange. It was proven in our previous experiment that the parenchyma cells of the PBZ-treated leaves were tightly packed because the decreased leaf size forced these tissues into such an arrangement (Ahmad Nazarudin et al. 2015). Fortunately, reduction in the transpiration rate and stomatal conductance could protect the plant against abiotic stresses related to water limitations or drought incidents. It could possibly decrease the amount of water lost through stomata. Fletcher et al. (2000) stated that triazole-treated plants had lower transpiration, required less water, and were able to adapt better to drought than untreated plants. In addition, KNO3, which supplies potassium, may also be beneficial in other aspects of plant biochemical processes, such as activating enzymes, regulating osmosis, and transporting photosynthates in the plant. As a consequence, the treated trees have greater tolerance to environmental stresses. Thus, PBZ and KNO3 may help protect this species when it is planted in harsh urban areas that expose it to the above-mentioned limitations.

CONCLUSION

In conclusion, the presence of PBZ produced a more compressed arrangement of cells in the leaves. Darker green leaves were observed due to enhanced relative chlorophyll content following PBZ and KNO3 treatment. The combination of PBZ and KNO3 also dramatically increased the leaf thickness of X. chrysanthus. In addition, reduced physiological attributes of photosynthetic and transpiration rates and stomatal conductance were found in the presence of PBZ. Reduction of the physiological capacity would reduce the amount of water loss through transpiration and help to enhance the water-holding ability of the leaves. Thus, PBZ would be beneficial for trees planted in harsh urban settings, which usually experience water constraints due to improper soil conditions, drought, and heat. This study recommends the combination of PBZ and KNO3 as one of the treatments for X. chrysanthus under local climatic conditions where improved tolerance to environmental stresses is desired.

ACKNOWLEDGMENTS

The authors gratefully acknowledge the Ministry of Agriculture and Agro-Based Industry Malaysia for financial support (05-03-10-SF1030). Thanks to Rosfarizal Kamaruzaman and Mohd Rizal Kasim for their technical assistance. We acknowledge the KLCH for site permission.

Footnotes

  • Conflicts of Interest:

    The authors reported no conflicts of interest.

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Changes in Leaf Thickness, Chlorophyll Content, and Gas Exchange of a Landscape Tree, Xanthostemon chrysanthus, Treated with Paclobutrazol and Potassium Nitrate
Ahmad Nazarudin Mohd Roseli, Tsan Fui Ying, Normaniza Osman
Arboriculture & Urban Forestry (AUF) Mar 2021, 47 (2) 53-63; DOI: 10.48044/jauf.2021.005
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