Functional Traits of Stem and Leaf of Wrightia …philjournalsci.dost.gov.ph/images/pdf/pjs_pdf/vol148no2/...both W. candollei and P. indicus have dorsiventral leaf, wavy or V-shaped

Keywords: anatomy, endemic, functional traits, native species, restoration

Functional Traits of Stem and Leaf of Wrightia candollei S. Vidal

1Department of Forest Biological Sciences, College of Forestry and Natural Resources (CFNR) University of the Philippines Los Baños (UPLB), College, Laguna 4031 Philippines

2College of Agriculture, Southern Luzon State University Lucban, Quezon, Philippines

*Corresponding author: [email protected]

Jonathan O. Hernandez1, Marilyn O. Quimado1, Edwino S. Fernando1, Dennis E. Pulan2, Pastor L. Malabrigo Jr.1, and Lerma S.J. Maldia1

Morpho-anatomical functional traits of native tree species are deemed important in forest restoration. Although much is known about morpho-anatomical traits of many terrestrial plants, such traits in Philippine native trees remain unclear. In this study, the stem and leaf morpho-anatomy of W. candollei S. Vidal was investigated to provide insights on its potential for restoration of dry, degraded lands. Results suggest that the morpho-anatomical structure of leaf and stem of W. candollei conforms to characteristics typical of plants adapted to dry areas and to species commonly used for restoration. The presence of trichomes, multiple layers of storage cells and mechanical cells, sclerenchymatic phloem cap, multiple vascular bundles, living xylem parenchyma, and steep leaf inclination were observed and interpreted as important leaf and stem structural traits of W. candollei. These morpho-anatomical traits are commonly associated with (1) solar radiation and water loss reduction; (2) tissue/organ mechanical reinforcement; and (3) water uptake and storage. Therefore, W. candollei – in association with the other native species – might be potentially useful for restoration of dry degraded lands in the Philippines. However, ecophysiological and phenological studies, as well as watering regime experiments, are recommended to better understand the actual habitat preference of the species.

Philippine Journal of Science148 (2): 301-308, June 2019ISSN 0031 - 7683Date Received: 23 Aug 2018

INTRODUCTIONThe restoration of heavily degraded areas has become one of the emerging research interests across tropical countries. In the Philippines, two of the important observations noted from restoration efforts are (1) the selection of appropriate forest tree species and (2) their suitability to open-field conditions (Chechina and Hamann 2015). The selection of species for restoration of degraded lands is considered a complex task. Forest ecologists recommend native species for forest restoration because it is the best way to restore dry degraded lands’ ecological integrity into its original state. Native tree species may also have morpho-anatomical functional and

adaptive traits that exotic species widely used for restoration may also have, allowing them to adapt to dry degraded environment. These traits have long been studied for many plants from the tropics. However, because plant responses to environmental stress are complex, the functions of these morpho-anatomical traits are still unknown to Philippine native trees in the context of forest restoration.

Every organ of a plant has important functions to fulfill all the metabolic and physiological processes in a particular environment. Plant’s survival should depend on the ability to match anatomical structures and functions to withstand desiccation (Maximov and Yapp 1929). For instance, species in arid areas showed specific adaptive

301

traits and mechanisms against dry conditions (Hernandez et al. 2016, Polle and Chen 2014). The examples of these mechanisms are leaf shedding, decrease in leaf number and size and branches, thick cuticle and epidermal cell walls, and additional layers of palisade parenchyma (De Micco and Aronne 2012). The presence of trichomes was also found to have useful role in attracting pollinators, as defense against herbivores and pathogen attacks (Milan et al. 2006), and in water storage (Bandyopadhyay et al. 2004). These features are mainly linked to increased water uptake and storage, reduction of water loss, and mechanical reinforcement of tissues to prevent wilting (De Micco and Aronne 2012). In addition, many studies reported the molecular basis of morpho-anatomical traits in plants (Ning et al. 2016, Polle and Chen 2014, Serna and Martin 2006, Esch et al. 2004, Chaves et al. 2003), and hundreds of genes that are induced by environmental stresses (e.g., drought) have already been identified (Chaves et al. 2003).

In this study, the morpho-anatomical functional traits of Wrightia candollei (Apocynaceae) and Pterocarpus indicus (Fabaceae) were investigated. W. candollei is a small, deciduous tree species endemic to the Philippines. It is common in deciduous lowland tickets and coastal forests of Benguet, Pangasinan, Zambales, Nueva Ecija, Rizal, Laguna, Mindoro, and Palawan. In addition, the conservation status of W. candollei has not yet been assessed (Villanueva and Buot 2015). On the other hand, Pterocarpus indicus is a semi-deciduous species – a widely used reforestation tree species in the Philippines (Delos Reyes et al. 2016, Finkeldey et al. 1999). It has a wide range of distribution in the country, which behaves like a pioneer species and grows best in open conditions (Orwa et al. 2009).

The objectives of the present study were: (a) to examine the stem and leaf morpho-anatomy of W. candollei in comparison to a widely distributed and commonly planted native forest tree species, Pterocarpus indicus Willd.; and (b) to provide insights on how these traits may play important roles in adapting and restoring dry degraded lands in the Philippines.

MATERIALS AND METHODS

Preparation of SpecimensYoung stem and leaf samples of W. candollei (Figure 1) and P. indicus were collected from a dry coastal forest in Lobo, Batangas at 600 m above sea level and from Mt. Makiling Forest Reserve, Philippines. From each species, five individuals were selected and leaf samples (one per individual) were cut from the third leaf of the orthotropic

branch. A cross-section of approximately 1–2 mm x 2–3 mm leaf samples from the middle portion of midrib were obtained. For stem sample, ca. 1–2 mm long was cut transversely.

Microscopic Examination and AnalysisExamination of leaf and stem tissues was done using paraffin-embedded samples following the procedures of Johansen (1940). To examine the stomata of the two species, the freehand technique through epidermal impression was used. The area of stomata (square microns) was measured using the image processing and analysis software (ImageJ version 1.51k). A 51,300-µm2 grid was used to measure the size of stomata following the procedure of Xu and Zhou (2008). All the anatomical structures observed in the cross-sections of leaf and stem were identified following the typologies described in Metcalfe and Chalk (1959).

Measurements of thickness and counts of a number of layers of cells and tissues were done using a compound microscope (Euromex 0112987, Blueline Holland) under 10X magnification. The mean thickness (µm) and area (µm2) of leaf anatomical tissues were computed using R-studio Statistical Package software version 3.4.0. A total of 19 leaf and stem characters were used to determine and analyze the percent similarity of W. candollei and P. indicus using the UPGMA clustering method in PAST version 3.14.

Pterocarpus indicus is a semi-deciduous species – a widely used reforestation tree species in the Philippines (Delos Reyes et al. 2016, Finkeldey et al. 1999). It has a wide range of distribution in the country, which behaves like a pioneer species and grows best in open conditions (Orwa et al. 2009).

Figure 1. Leaf and stem of (a–b) Wrightia candollei and (c) Pterocarpus indicus collected from Lobo, Batangas, the Philippines at 600 m above sea level. The bar represents 10 cm.

Hernandez et al.: Wrightia candollei S. VidalPhilippine Journal of ScienceVol. 148 No. 2, June 2019

302

RESULTS

Morpho-anatomical CharacteristicsThe comparative stem and leaf morpho-anatomical features of W. candollei and P. indicus are shown in Figures 2–6. The UPGMA clustering method clearly showed that W. candollei and P. indicus are about 87% similar in terms of morphological and anatomical characters. The data matrix used in cluster analysis is presented in Table 1.

In the stem, both species have an angular stem, uniserate epidermis, parenchymatic cortical layer, and collenchymatic hypodermis (Fig. 2). The epidermis enclosed several cortex cells, which is built up of thin-walled parenchyma cells. Sclerenchymatic phloem cap was observed in both species but is more prominent in P. indicus (Fig. 2). Lastly, both species have living xylem parenchyma in the vascular bundles. In terms of arrangement, these vascular bundles are of the amphicribral type in both species.

Figure 2. Stem anatomy of (a–b) W. candollei and (c–d) P. indicus showing pa (parenchyma), co (collenchyma), sc (sclerenchymatic phloem cap), xy (xylem), ph (phloem), xp (xylem parenchyma), ep (epidermis), and tr (trichome).

The leaf anatomical structures of W. candollei and P. indicus are presented in Figure 3. This figure shows that both W. candollei and P. indicus have dorsiventral leaf, wavy or V-shaped blade inclination, uniseriate upper and lower epidermises, 1–2 layers of elongated palisade mesophyll cells, irregularly shaped spongy mesophyll with conspicuous intercellular spaces, and convex-shaped midrib (Fig. 3).

Figure 4. Range and mean thickness values of (a) simple tissues in stem, (b) leaf upper and lower epidermises, (c) vascular tissues in stem and leaf, and (d) leaf mesophyll tissues.

Figure 3. Leaf anatomy of (a–b) W. candollei and (c–d) P. indicus showing pa (parenchyma), co (collenchyma), pm (palisade mesophyll), sm (spongy mesophyll), xy (xylem), ph (phloem), ep (epidermis), and tr (trichome).

The thickness of the observed leaf and stem tissues is shown in Figure 4. In the stem, there was no much difference found in the thickness of their open collateral vascular bundles, xylem and phloem conduits, and cell wall of vessels (Fig. 4). One significant observation is that W. candollei has a higher number of vascular bundles than P. indicus. In the leaf, W. candollei has bigger midrib (1,143.70 ± 25.0 µm) than that of P. indicus (606.05 ± 13.13 µm). However, both midribs have collenchymatic adaxial surface. In W. candollei, 3–5 layers of collenchyma and 5–12 layers of parenchyma cells were also observed in the abaxial surface of the midrib (Fig. 4).


303

Table 1. Matrix of leaf and stem morpho-anatomical characteristics of W. candollei and P. indicus used in cluster analysis to determine their percent similarity.

Characters W. candollei P. indicus

Leaf

Convex midrib + +

Dorsiventral leaf + +

Leaf inclination + +

1–2 layers palisade mesophyll cells + –

Irregularly shaped spongy mesophyll cells – +

Uniseriate upper and lower epidermis + +

Capitate trichomes + +

Branched trichomes + –

Cylindrical/conical trichomes + +

Parenchymatic midrib + +

Collenchymatic midrib + –

Paracytic stomata + +

Stem

Peltate trichomes + –

Cylindrical/conical trichomes + +

Circular to slightly angular stem shape + +

Sclerenchymatic phloem cap + +

Collenchymatic hypodermis + +

Angular collenchyma + –

Open collateral vascular bundles + +

Figure 5. Trichomes of W. candolleii showing (a) peltate, (b) stellate, (c) branched, and (d) uniseriate cylindrical trichomes (d); and of P. indicus showing (e) uniseriate conical and (f) capitate trichomes. The bar represents 10 µm.

Epidermal Characteristics The different types and structure of trichomes are shown in Figure 5. Both stems and leaves of the two studied taxa are covered with trichomes but are more abundant in W. candollei. Four types of trichomes were observed in W. candollei, namely peltate (with stalk and a flat disk-shaped top); stellate trichomes (branched at the tip forming a star-shape protuberance); and branched (have one major stalk, 15–25 µm long and 5–6 branches, 15–25 µm long) resembling a twig; and uniseriate cylindrical trichomes. These trichomes are structurally distributed on different surfaces of the leaf and stem (20–35 µm long). The cylindrical trichomes are the most prominent type on both adaxial (i.e., 101 trichomes/mm2) and abaxial surfaces (i.e., 105 trichomes/mm2) of the leaf. A high number of stellate trichomes was also observed on the abaxial surface of the leaf (i.e., 89 per mm2) of W. candollei. Branched and peltate trichomes were only observed on the outer surface of the primary and secondary veins of W. candollei. In P. indicus leaf, only two types of trichomes were observed, namely: uniseriate conical trichomes (38–40 µm long), capitate with 30–35 µm long stalk, and round-shaped top (Figs. 5e–f). Both types of trichomes were observed on stem and leaf of P. indicus, but more conical trichomes were observed on the abaxial surface of the leaf (i.e., 50–80 trichomes/mm2). The stem and midrib of the leaf of P. indicus are mostly covered with capitate trichomes (70–100 trichomes/mm2).

Lastly, both species have paracytic stomata wherein two subsidiary cells are parallel to the long axis of the guard cells (Fig. 6). The stomata of W. candollei are elliptical-shaped (0.80–0.91µm) with convex guard cells leveled with the surface, which is bigger than that of P. indicus (0.30–0.50µm).

Figure 6. Paracytic stomata of (a) W. candollei and (b) P. indicus. The bar represents 10 µm.

DISCUSSIONThis study reports for the first time the conformity of most of the stem and leaf morpho-anatomical traits of W. candollei to the anatomy of widely adapted forest trees species such as P. indicus. In this study, we show that the presence of trichomes, multiple layers of storage cells and mechanical cells, sclerenchymatic phloem cap, living xylem parenchyma, multiple vascular bundles, and steep leaf inclination might be important leaf and stem


304

functional traits of W. candollei. The sclerenchymatic phloem cap and xylem and phloem parenchyma observed in W. candollei were reported as important structural traits of fast-growing species such as Gmelina arborea (Moya and Fo 2007, Plomion et al. 2001) and Leucaena leucocephala (El-Lamey 2015). This suggests that W. candollei have morpho-anatomical similar in species widely used for reforestation, which are adapted to a wide range of environments. Hence, we hypothesized that W. candollei may be capable of withstanding dry degraded conditions through the help of these morpho-anatomical traits. We grouped these traits into three functional strategies, which are mainly linked to (1) solar radiation regulation, water loss reduction, and photosynthesis augmentation; (2) tissue/organ mechanical reinforcement; and (3) water uptake and storage.

Solar Radiation Regulation, Water Loss Reduction, and Photosynthesis AugmentationThe first remarkable result of this study is the clear steep leaf inclination of W. candollei related to solar radiation, water loss reduction, and photosynthesis rate augmentation. This functional trait may have important photoprotection roles for W. candollei. It can be an added mechanism of W. candollei in altering the total light interception and seasonal variations of irradiances that strike on its trichomous leaf surface. This may allow species to change its leaf inclination to horizontal/vertical orientation depending on the degree of available solar radiation. Presumably, W. candollei (a deciduous tree) may either shed leaves or exhibit foliage inclination to continue photosynthesis while preventing water loss through transpiration during water deficit. We hypothesized that the photosynthesis rate in W. candollei could be maintained when the orientation of its leaf changes. This is because as the leaf orientation changes, the chloroplasts may move from low-light to high-light exposed areas. Valladares and Pearcy (1998) reported that foliage-inclination is useless in low-light exposed leaves. In fact, summer and semi-deciduous dimorphic species have leaves and other photosynthetic surfaces that modify the angle/orientation to avoid photosystems damage (Gratani and Bombelli 2000). This allows the optimization of light interception during early morning and late afternoon, thereby reducing solar radiation at midday (Aronne 2001). In addition to leaf inclination, the stem of other plants retains green to maintain photosynthesis (Gibson 1983). Leaf inclination observed in W. candollei follow the reported characteristics of plants occurring in dry habitats (Arena et al. 2008) and even in cold conditions (Oliveira and Peñuelas 2002). At the molecular level, multiple genetic loci that regulate leaf inclination angle attributed to positive plant performance, avoidance of heat stress, and maximization of carbon gain were reported in many

studies (Truong et al. 2015, Chaves et al. 2003, Zanten et al. 2010, Havaux and Tardy 1999).

In this study, the presence of different types of trichomes was also interpreted as one of the important functional leaf traits of W. candollei in reducing water loss and solar radiation. Trichomes are known for their role in the physical protection of plants against abiotic stresses such as high light intensity and temperatures. The highly dense distribution of cylindrical trichomes on both surfaces of the leaf may create added efficient protection against intense solar radiation, thereby reducing water loss during transpiration. Recently, the trichome-related gene expression of ecological adaptation of species under low precipitation conditions was reported by Ning et al. (2016). It was found out that GIS2, TTG1, and GL1 were the key positive-regulated genes involved in trichome initiation and development in Caragana korshinskii (commonly used to improve drought ecosystems in Central China). These genes were linked to drought resistance properties of the species. Similarly, a study of Ichie et al. (2016) found that species with various types of trichomes had significant intrinsic water use efficiency (WUE) – one of the comprehensive indicators of H2O and CO2 assimilation to produce organic matter. Further, a recent study of Cardoso-Gustavson et al. (2014) showed that trichomes produce hydrophilic substances that can prevent desiccation, maintain adequate moisture in the leaf, and favor leaf growth.

Water losses are also a function of the characteristics of stomata. The paracytic stomata may also have important adaptation role for W. candollei. This type of stomata of W. candollei was also observed in the leaf of Myrceugenia rufa (Myrtaceae) – an endemic coastal shrub of north-central Chile (Retamales et al. 2015). Leaves with such type of stomata were linked to the plant’s adaptations for populating high light and water-limited habitats (Nikolova and Vassilev 2011). The observed measurements were far smaller than what was reported as “small’ stomatal size of trees (Rossatto and Kolb 2010). Size of stomata is also associated with plant’s adaptations to various habitats. However, we recommend further studies to validate whether the stomatal size observed in W. candollei is a functional trait using more samples of leaves subjected to environmental manipulations (e.g., light intensity, water availability, and temperature). According to Kröber et al. (2015), stomatal density is more of a plastic response to environmental changes while the size of stomata may be attributed to plant’s adaptation to drought. Similarly, Shields (1950) mentioned that plants with small stomata are likely to occur in environments with high luminosity and low humidity, which are assumed to be features of xeromorphic leaves. In contrast with Yadollahi et al. (2011), the stomatal size and density were reported as


305

fixed even after resizing in new leaves. In addition, drawn from the plant-water relations theory, smaller stomata may pose efficiency in the use of water resources. The stomata of W. candollei are not sunken, but these pores may be well-protected by a dense covering of different types of trichomes. Such feature may even decrease the temperature in leaves and thereby reducing water loss.

Tissue/organ Mechanical ReinforcementThe function of trichomes in the leaf of W. candollei could not be restricted to water retention and solar radiation reduction. The study found the dense distribution of trichomes in leaf even after a tedious and series of procedures of the histological paraffin technique. Presumably, fibrous trichomes of the species may function for leaf tissue mechanical reinforcement. This trait would suggest a protective function for W. candollei against herbivores and pathogen attack. This would also protect the leaf (a very important photosynthetic organ) from rupture during heavy rain and strong wind in the environment. This protection provided by the trichomes may also be true to the stem of W. candollei, protecting the stem (especially young stem) from any form of disturbance. This observation was based on on the fact that one significant role of trichomes is to protect plant organs against harsh environments (Werker 2000).

Further, the observed multiple layers of thick-walled cells (sclerenchyma and collenchyma) in the midrib and stem of W. candollei may also give firmness or mechanical support for the species. De Micco and Aronne (2012) reported the presence of multiple layers of collenchyma cells as characteristics of plants occurring in arid areas. Hence, during dry periods which may be encountered by W. candollei, this trait may prevent the collapse of tissues and cells. This collapse can trigger the loss of functionality in the absence of adequate moisture in the environment.

Water Uptake and StorageThe multiple layers of storage cells (parenchyma) and vascular bundles in stem and midrib may help W. candollei increase water uptake and storage. These features were described as an important adaptation for xeric habitats (Garcia et al. 2012). The development of multiple layers of vascular bundles, which are major components of wood (Raven et al. 1976), is essential to plants thriving in terrestrial environments (Carland et al. 1999). Janz et al. (2012) discovered that transcript abundances of genes active during tension wood formation were suppressed in the xylem of a salt-tolerant species (typical of dry areas), whereas those for stress and defense-related genes increased. This resulted in hydraulic adaptation by an alteration of vessel densities and frequencies. Sack and Scoffoni (2013) claimed that a higher number of vessels

can contribute to higher leaf hydraulic conductance (Kleaf). The authors further noted that a higher number of phloem can contribute to faster phloem transport rates.

Multiple vascular bundles in W. candollei can be enhanced by the presence of sclerenchymatic phloem cap and xylem parenchyma cells. Sack and Scoffoni (2013) reported that such characteristics can improve resistance to shrinkage during dehydration. In addition, thick layers of parenchyma cells may play an important role in water storage for the species. Under conditions of water scarcity, plants can utilize the water stored from the parenchyma cells. Its thin-walled characteristic can make cells shrink easily when water is not available, but can immediately recover when favorable conditions are restored. This feature of parenchyma cells has been reported in plants in arid areas (De Micco and Aronne 2012). In addition, in a young cross-section of the stem of W. candollei, xylem parenchyma is also very evident, which may function for water storage. Its strategic location near the vessels and phloem cells can regulate the transport of water from roots to leaves and other parts of the plant. The insights we present in this study has long been proven by an experiment on parenchyma-chlorenchyma water movement during drought (Nobel 2006). The author noted that water stored from the parenchyma cells may shift to chlorenchyma cells (more chloroplast therein) to maintain a positive CO2 rate during drought condition.

In conclusion, the stem and leaf anatomy of W. candollei exhibit morpho-anatomical functional traits typical of plants that thrive in arid conditions and of widely-used species for reforestation such as P. indicus. These leaf and stem functional traits were interpreted as beneficial for water uptake and storage, solar radiation and water loss reduction, photosynthesis augmentation, and tissue/organ mechanical reinforcement of W. candollei. Combinations of these traits can contribute to the adaptive capacity of W. candollei to a dry degraded environment. Therefore, W. candollei may be a potential native tree species for restoration of degraded lands – especially dry coastal ecosystems in association with other widely-used reforestation species. However, ecophysiological and phenological studies, as well as watering experiments, are recommended to better understand its actual habitat preference.

ACKNOWLEDGMENTThe authors would like to thank the Metallophytes Laboratory at the CFNR-UPLB for providing the team with all the necessary materials and equipment in the conduct of the present study. We also thank the Philippine Forest Foundation for providing us the budget to conduct an important section of the study.


306

REFERENCESARENA C, VITALE L, SANTO AV. 2008. Paraheliotropism

in Robinia pseudoacacia L.: An efficient strategy to optimize photosynthetic performance under natural environmental conditions. Plant Biology 10(2): 194–201. doi:10.1111/j.1438-8677.2008.00032.x

ARONNE G. 2001. Seasonal Dimorphism in the Mediterranean Cistus incanus L. subsp. incanus. Annals of Botany 87(6): 789–794. doi:10.1006/anbo.2001.1407

BANDYOPADHYAY T, GANGOPADHYAY G, PODDAR R, MUKHERJEE KK. 2004. Trichomes: Their Diversity, Distribution, and Density in Acclimatization of Teak (Tectona grandis L.) Plants Grown in vitro. Plant Cell, Tissue and Organ Culture 78(2): 113–121. doi:10.1023/b:ticu.0000022534.03276.c5

CARDOSO-GUSTAVSON P, CAMPBELL LM, MAZZONI-VIVEIROS SC, DE BARROS F. 2014. Floral colleters in Pleurothallidinae (Epidendroideae: Orchidaceae). American Journal of Botany 101: 587–597.

CARLAND FM. 1999. Genetic Regulation of Vascular Tissue Patterning in Arabidopsis. The Plant Cell Online 11(11): 2123–2138. doi:10.1105/tpc.11.11.2123

CHAVES MM, MAROCO JP, PEREIRA JS. 2003. Understanding plant responses to drought—from genes to the whole plant. Functional Plant Biology 30(3): 239. doi:10.1071/fp02076

CHECHINA M, HAMANN A. 2015. Choosing species for reforestation in diverse forest communities: Social preference versus ecological suitability. Ecosphere 6(11). doi:10.1890/es15-00131.1

DELOS REYES MT, MAGPANTAY GD, CAGALAWAN AJ, LAPIS AB, CALINAWAN NM. 2016. Assessment of Genetic Diversity of Narra (Pterocarpus indicus Willd.) Populations from Various Seed Sources in the Philippines using RAPD. Journal of Environmental Science and Management 19(2): 54–63.

DE MICCO VD, ARONNE G. 2012. Occurrence of Morphological and Anatomical Adaptive Traits in Young and Adult Plants of the Rare Mediterranean Cliff Species Primula palinuri Petagna. The Scientific World Journal. p. 1–10. doi:10.1100/2012/471814

EL-LAMEY TM. 2015. Morphological and Anatomical Responses of Leucaena leucocephala (Lam.) de Wit. and Prosopis chilensis (Molina) Stuntz to Ras Sudr Conditions. Journal of Applied Environmental and Biological Sciences 5(7): 43–51.

ESCH JJ, CHEN M. A, HILLESTAD M, MARKS MD. 2004. Comparison of TRY and the closely related

At1g01380 gene in controlling Arabidopsis trichome patterning. The Plant Journal 40(6): 860–869. doi:10.1111/j.1365-313x.2004.02259.x

FINKELDEY R, GUZMAN ND, CHANGTRAGOON S. 1999. The Mating System of Pterocarpus indicus Willd. at Mt. Makiling, Philippines. Biotropica 31(3): 525-530. doi:10.1111/j.1744-7429.1999.tb00397.x

GARCIA JD, SCREMIN-DIAS E, SOFFIATTI P. 2012. Stem and root anatomy of two species of Echinopsis (Trichocereeae, Cactaceae). Revista Mexicana De Biodiversidad 83(4). doi:10.7550/rmb.28124

GIBSON AC. 1983. Anatomy of photosynthetic old stems of nonsucculent dicotyledons from North American deserts. Botanical Gazette 144: 347–363.

GRATANI L, BOMBELLI A. 2000. Correlation between leaf age and other leaf traits in three Mediterranean maquis shrub species: Quercus ilex, Phillyrea latifolia, and Cistus incanus. Environmental and Experimental Botany 43(2): 141–153. doi:10.1016/s0098-8472(99)00052-0

HAVAUX M, TARDY F. 1999. Loss of chlorophyll with limited reduction of photosynthesis as an adaptive response of Syrian barley landraces to high-light and heat stress. Functional Plant Biology 26(6): 569. doi:10.1071/pp99046

HERNANDEZ JO, MALABRIGO PL, QUIMADO MO, MALDIA LSJ, FERNANDO ES. 2016. Xerophytic characteristics of Tectona philippinensis Benth. & Hook.f. Philippine Journal of Science 145(3): 259–269.

ICHIE T, INOUE Y, TAKAHASHI N, KAMIYA K, KENZO T. 2016. Ecological distribution of leaf stomata and trichomes among tree species in a Malaysian lowland tropical rain forest. Journal of Plant Research 129(4): 625–635. doi:10.1007/s10265-016-0795-2

JANZ D, LAUTNER S, WILDHAGEN H, BEHNKE K, SCHNITZLER J, RENNENBERG H, POLLE A. 2012. Salt stress induces the formation of a novel type of ‘pressure wood’ in two Populus species. New Phytologist 194(1): 129–141. doi:10.1111/j.1469-8137.2011.03975.x

JOHANSEN DA. 1940. Plant Microtechnique. New York: McGraw-Hill Book Co. p. 126–156.

KRÖBER W, PLATH I, HEKLAU H, BRUELHEIDE H. 2015. Relating Stomatal Conductance to Leaf Functional Traits. Journal of Visualized Experiments No. 104. doi:10.3791/52738

MAXIMOV NA, YAPP RH. 1929. The plant in relation to water. London: George Allen & Unwin.


307

METCALFE CR, CHALK L. 1959. Anatomy of Dicotyledons – Leaves, Stem, and Wood in Relation to Taxonomy. Oxford: Clarendon Press.

MILAN P, HAYASHI AH, APPEZZATO-DA-GLÓRIA B. 2006. Comparative leaf morphology and anatomy of three Asteraceae species. Brazilian Archives of Biology and Technology 49(1): 1352015. Relating Stomatal Conductance to Leaf Functional Traits 144. doi:10.1590/s1516-89132006000100016

MOYA R, FO MT. 2006. Variation in the wood anatomical structure of Gmelina arborea (Verbenaceae) trees at different ecological conditions in Costa Rica. Revista De Biología Tropical 56(2): 689–704. doi:10.15517/rbt.v56i2.5617

NING P, WANG J, ZHOU Y, GAO L, WANG J, GONG C. 2016. Adaptional evolution of trichome in Caragana korshinskii to natural drought stress on the Loess Plateau, China. Ecology and Evolution 6(11): 3786–3795. doi:10.1002/ece3.2157

NIKOLOVA A, VASSILEV A. 2011. A Study on Tribulus terrestris L. Anatomy and Ecological Adaptation. Biotechnology & Biotechnological Equipment 25 (2): 2369–2372.

NOBEL PS. 2006. Parenchyma-chlorenchyma Water Movement during Drought for the Hemiepiphytic Cactus Hylocereus undatus. Annals of Botany 97(3): 469–474. doi:10.1093/aob/mcj054

OLIVEIRA G, PEÑUELAS J. 2002. Comparative protective strategies of Cistus albidus and Quercus ilex facing photoinhibitory winter conditions. Environmental and Experimental Botany 47(3): 281–289. doi:10.1016/s0098-8472(02)00003-5

ORWA C, MUTUA A, KINDT R, JAMNADASS R, ANTHONY S. 2009. Agroforestree Database: A tree reference and selection guide version 4.0. Retrieved from http://www.worldagroforestry.org/sites/treedbs/treedatabases.asp

PLOMION C, LEPROVOST G, STOKES A. 2001. Wood Formation in Trees. Physiology 127: 1513–1523.

POLLE A, CHEN S. 2014. On the salty side of life: Molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant, Cell & Environment 38(9): 1794–1816. doi:10.1111/pce.12440

RAVEN PH, EVERT RF, CURTIS H. 1976. Biology of Plants. New York: Worth Publishers.

RETAMALES HA, CABELLO A, SERRA MT, SCHARASCHKIN T. 2015. Leaf micromorphology and anatomy of Myrceugenia rufa (Myrtaceae). An

endemic coastal shrub of north-central Chile. Gayana Botánica 72(1): 76–83. doi:10.4067/s0717-66432015000100010

ROSSATTO DR, KOLB RM. 2010. Gochnatia polymorpha (Less.) Cabrera (Asteraceae) changes in leaf structure due to differences in light and edaphic conditions. Acta Botanica Brasilica 24(3): 605–612. doi:10.1590/s0102-33062010000300002

SACK L, SCOFFONI C. 2013. Leaf venation: Structure, function, development, evolution, ecology, and applications in the past, present, and future. New Phytologist 198(4): 983–1000. doi:10.1111/nph.12253

SERNA, L , MARTIN C. 2006 . Tr i chomes : Different regulatory networks lead to convergent structures. Trends in Plant Science 11(6): 274–280. doi:10.1016/j.tplants.2006.04.008

SHIELDS LM. 1950. Leaf xeromorphy as related to physiological and structural influences. The Botanical Review 16(8): 399–447. doi:10.1007/bf02869988

TRUONG SK, MCCORMICK R. F, ROONEY W.L, MULLET JE. 2015. Harnessing Genetic Variation in Leaf Angle to Increase Productivity of Sorghum bicolor. Genetics 201(3): 1229–1238. doi:10.1534/genetics.115.178608

VALLADARES F, PEARCY RW. 1998. The functional ecology of shoot architecture in some sun and shade plants of Heteromeles arbutifolia M. Roem., a California chaparral shrub. Oecologia 114: 1–10.

VILLANUEVA EL, BUOT JI. 2015. Threatened Plant Species of Mindoro, Philippines. IAMURE International Journal of Ecology and Conservation 14(1). doi:10.7718/ijec.v14i1.901

WERKER E. 2000. Trichome diversity and development. Advances in Botanical Research 31: 1–35.

XU Z, ZHOU G. 2008. Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. Journal of Experimental Botany 59(12): 3317–3325. doi:10.1093/jxb/ern185

YADOLLAHI A, ARZANI K, EBADI A, WIRTHENSOHN M, KARIMI S. 2011. The response of different almond genotypes to moderate and severe water stress in order to screen for drought tolerance. Scientia Horticulturae 129(3): 403–413. doi:10.1016/j.scienta.2011.04.007

ZANTEN MV, PONS TL, JANSSEN JA, VOESENEK LA, PEETERS AJ. 2010. On the Relevance and Control of Leaf Angle. Critical Reviews in Plant Sciences 29(5): 300–316. doi:10.1080/07352689.2010.502086


308

Functional Traits of Stem and Leaf of Wrightia …philjournalsci.dost.gov.ph/images/pdf/pjs_pdf/vol148no2/...both W. candollei and P. indicus have dorsiventral leaf, wavy or V-shaped

Documents