What is new in boron nutrition? Case study on African mahogany leaf anatomy

ABSTRACT

Fertilization with boron (B) is a crucial aspect in the management of tropical soils to achieve high yield and wood quality in forest species. However, studies are still needed for a better understanding of the effects of B on the anatomy and physiology of African mahogany to improve borate fertilization programs in terms of doses and sources of B. The objective was to characterize the morphology and anatomy of African mahogany leaves subjected to doses and sources of B, as well as to investigate leaf lesions caused by excess B. In a 3 × 3 factorial scheme, a randomized block design was used with four replications, resulting in a total of 36 experimental units. The treatments consisted of three sources of B: borax (sodium tetraborate), ulexite, and colemanite, and three doses of B: 0, 1.5, and 3 mg dm ^–3 . After 120 days of transplanting, leaf samples with and without toxicity lesions were collected for morphological and anatomical evaluations. Following the collection, the samples were photographed and fixed in Karnovsky’s solution. The plants cultivated in the control treatment did not exhibit any symptoms of B deficiency in the leaf tissue. Borax and ulexite sources, and higher doses of B resulted in greater lesions, accompanied by the accumulation of phenols in the necrotic region. In contrast, the source of lower solubility (colemanite) and lower dose of B demonstrated the highest accumulation of starch. African mahogany is sensitive to applying high doses (3 mg dm ^–3 ) and high solubility sources of Boron (borax). Excessive B levels cause necrosis and structural disorganization of African mahogany leaf tissues.

histopathology; micronutrient; morphology

Introduction

The African mahogany ( Khaya grandifoliola (C.) DC.) is a timber species with great significance in the global market, mainly due to its high commercial value in the international hardwood market (Ribeiro et al., 2017). The species is commonly known as green gold and is used in various applications, including lamination, luxury furniture, interior construction, and shipbuilding (Alves Júnior et al., 2017).

It is of paramount importance to give special attention to the nutritional management of the forest if the objective is to achieve high yield and wood quality. This encompasses the assertive choice of fertilizers and nutrient doses. Among the essential elements for plant development, boron (B), along with calcium (Ca), is of particular importance in influencing wood quality. In the plant, B plays a vital role in structuring the cell wall and forming new tissues (Marschner, 2012). B-deficient forests exhibit several undesirable conditions for sawmills, including death of the apical meristem, excessive budding of lateral buds, and trunk tortuosity (Marschner, 2012).

Boron is known to exhibit a close relationship between adequate and toxic levels (Marschner, 2012). In some species, such as Eucalyptus spp., this relationship between adequate and toxic levels is somewhat more expansive (Marcar et al., 1999; Mattiello et al., 2009). However, in other species, the relationship is more finely balanced, as observed in species of the genus Khaya spp. (Araújo et al., 2017). Therefore, it is to monitor the quantity and solubility of the applied soil amendments to prevent the occurrence of physiological disorders and losses in productivity.

The literature reports the dynamics and importance of B in forest species (Zhou et al., 2012; Olykan et al., 2008). However, few studies have reported in detail the anatomical effects of B deficiency and/or toxicity on leaf tissues, and the information gap is even wider for species of the genus Khaya spp. Thus, anatomical description becomes essential to understand possible changes in plant tissues formation, organization, and structure subjected mainly to mineral fertilization with B (Rosolem and Leite, 2007).

The objective of this study was to assess the following hypotheses: a) Can high doses and more soluble sources of B result in greater proportions of anatomical changes? b) Can B deficiency result in malformation of plant cellular tissues? c) Can B toxicity promote cellular disorganization, resulting in specific changes?

The present study was conducted to characterize the anatomy of African mahogany leaves in response to sources and doses with differential solubility rates. Additionally, the occurrence of leaf lesions caused by B excess was investigated.

Materials and Methods

Experimental conditions

The experiment was carried out in a greenhouse at the Departamento de Ciências do Solo at the Escola Superior de Agricultura Luiz de Queiroz (ESALQ), Piracicaba, São Paulo state, Brazil (22°42’30” S, 47°38’00” W, altitude 570 m). The African mahogany species used was Khaya grandifoliola (Meliaceae) at 60 days of age. The seedlings were transplanted into containers with a capacity of 9 kg, with one seedling per pot. The pots were maintained at 60 % of the soil water retention capacity during the experimental period.

The substrate was a soil classified as Oxisol, collected from the 0-20 and 20-40 cm layers. In the physical-chemical analysis, at the 0-20 cm layer, the substrate exhibited the following initial values: pH (CaCl ₂ ) = 5.6; phosphor (P) (Resin) = 8 mg dm ^–3 ; potassium (K) = 2.5 mmol _c dm ^–3 ; calcium (Ca) = 22 mmol _c dm ^–3 ; magnesium (Mg) = 9 mmol _c dm ^–3 ; zinc (Zn) = 3.7 mg dm ^–3 ; iron (Fe) = 18 mg dm ^–3 ; manganese (Mn) = 40.5 mg dm ^–3 ; copper (Cu) = 16 mg dm ^–3 ; boron (B) = 0.2 mg dm ^–3 ; H + Al = 16 mmol _c dm ^–3 ; sum of bases (SB) = 33.5 mmol _c dm ^–3 ; base Saturation (V %): 68; cation exchange capacity (CEC) = 49.5 mmol _c dm ^–3 ; organic matter (OM) = 15 g dm ^–3 ; clay = 175; silt = 44; and sand = 781 g kg ^–1 .

In the 20-40 cm layer, the values were: pH (CaCl ₂ ) = 6.3; phosphorous (P) (Resin) = 6 mg dm ^–3 ; potassium (K) = 0.7 mmol _c dm ^–3 ; calcium (Ca) = 34 mmol _c dm ^–3 ; magnesium (Mg) = 8 mmol _c dm ^–3 ; zinc (Zn) = 2.1 mg dm ^–3 ; iron (Fe) = 9 mg dm ^–3 ; manganese (Mn) = 25.6 mg dm ^–3 ; copper (Cu) = 6.5 mg dm ^–3 ; boron (B) = 0.1 mg dm ^–3 ; H + Al = 11 mmol _c dm ^–3 ; sum of bases (SB) = 42.7 mmol _c dm ^–3 ; base saturation (V %): 61; cation exchange capacity (CEC) = 53.7 mmol _c dm ^–3 ; organic matter (OM) = 9 g dm ^–3 ; clay = 201 g kg ^–1 ; silt = 61 g kg ^–1 ; and sand = 738 g kg ^–1 .

The substrate exhibited an optimal base saturation and pH for cultivating forest species, so liming was not necessary (Silveira et al., 2000).

Experimental design and treatments

The experimental design was based on a randomized block design in a 3 × 3 factorial scheme, with four replications, resulting in 36 experimental units (seedlings). The treatments comprised three B sources: borax (high solubility, 15 % total B and 12 % water soluble B); ulexite (medium solubility, 10 % total B and 5 % water-soluble B); and colemanite (low solubility, 10 % total B and 3 % water-soluble B); and three doses of B: 0, 1.5, and 3 mg dm ^–3 .

Doses of nitrogen (N) (150 mg dm ^–3 ), phosphorus (P) (200 mg dm ^–3 ), potassium (K) (150 mg dm ^–3 ), sulfur (S) (50 mg dm ^–3 ), manganese (Mn) (3 mg dm ^–3 ), zinc (Zn) (5 mg dm ^–3 ), molybdenum (Mo) (0.1 mg dm ^–3 ), and copper (Cu) (1.5 mg dm ^–3 ) were added to all treatments to complement the fertilization. After 120 days of transplantation, two samples of composite leaves were collected for morphological and anatomical evaluation. Samples with and without lesions (toxicity symptoms) were used.

Measurements, harvesting, and analyses

Following collection, the samples were photographed and fixed in the Karnovsky’s solution (Karnovsky, 1965). The samples were then conditioned to a vacuum pump (0.1 mm Hg) for 10 min to remove the air in the intercellular spaces, thus facilitating fixation. Subsequently, the samples were dehydrated in an increasing ethylic series (10, 20, 30, 40, 50, 60, 70, and 100 %), each ethylic series requiring 10 min, resulting in a total dehydration time of 80 min. Finally, the samples were infiltrated with Technovit glycol-methacrylate resin and sectioned to a thickness of 5 µm.

The samples were stained with toluidine blue for the standard histological analyses (Sakai, 1973) and then subjected to histochemical tests for pectin, starch, and phenolic compounds (Marques and Nuevo, 2022; Marques and Soares, 2022). Following staining, the histological slides were mounted with synthetic resin (Entellan Merck), and images were captured using a scanning electron microscope (Zeiss, Axioscope). Finally, the photographic plates were edited on a computer using the computer program Corel Draw®.

The B content of the leaves was also analyzed. For this, the samples were dried at 65 °C for three days until reaching a constant dry matter weight. Then B was determined using the nitroperchloric digestion method and the reading was performed using Inductively Coupled Plasma Optical Emission Spectrometry (ICP-OES) (Malavolta et al., 1997).

Results

The African mahogany plants grown in the control treatment exhibited average levels of 34.6 mg kg ^–1 , while the plants grown with B application demonstrated an average level of 127.6 mg kg ^–1 at the dose of 1.5 mg dm ^–3 and 190.7 mg kg ^–1 at a dose of 3 mg dm ^–3 . The observed values infer that African mahogany is more sensitive to B application than eucalyptus, as the onset of B toxicity symptoms was observed at 127.6 mg kg ^–1 , indicating a closer relationship between toxic and optimal levels.

The epidermis was observed to be composed of tabular cells on both sides, with the cells on the adaxial face being larger than those on the abaxial face. The leaf was hypostomatic, exhibiting stomata only on the epidermis of the abaxial surface. The mesophyll is dorsiventral, comprising palisade parenchyma with a layer of elongated cells on the adaxial face and spongy parenchyma with five layers of cells facing the abaxial face (Figure 1A and B). In the mesophyll are idioblast-like cells that accumulate crystals of calcium oxalate. The vascular bundle is collateral. The cell walls contain pectin (Figure 1C), the cells do not accumulate phenols (Figure 1D), and transient starch may or may not occur (Figure 1E).

Figure 1
– A) Morphology and B-E) cross-sectional micrographs of healthy leaves of Khaya grandifoliola (C.) DC. A) healthy leaf overview; B) toluidine blue staining; C) ruthenium red; D) iodized zinc chloride; E) ferric chloride; Epi ada = adaxial epidermis; Epi aba = abaxial epidermis; PP = palisade parenchyma; SP = spongy parenchyma; VB = vascular bundle.

Samples infiltrated with toluidine blue, ruthenium red, and iodinated zinc chloride (Figure 1B-D) showed well-formed cells and structures with no evidence of hypertrophy, vascular bundles, or disruption to the palisade and spongy parenchyma. A small starch accumulation was also observed when the samples were infiltrated with ferric chloride (Figure 1E).

The results demonstrate that greater solubility and higher doses of B were associated with greater lesion formation and higher phenol accumulation (Figure 2A1-3). Conversely, starch accumulation was inversely correlated with solubility, with the lowest solubility (colemanite) and the lowest dose of B exhibiting the highest accumulation (Figure 2I3).

Figure 2
– Leaves of Khaya grandifoliola (C.) DC plants subjected to sources and doses of boron. A and F) Digital microscope analyses; Anatomical and histochemical analyses = other columns; B and G) staining with toluidine blue; C and H) ruthenium red; D and I) iodized zinc chloride; E and J) ferric chloride. The analyses indicated a gradient of necrosis, accumulation of phenols, starch, and hypertrophy as a function of the doses and solubility of the boron sources. A3) initial lesion (arrow); F2) initial lesion with a chlorotic halo (arrow); A1, A2, and F1) advanced lesion with intense necrosis (arrow); B1) Compromised palisade parenchyma, loss of stomata and region of cell necrosis close to a vascular bundle (*). C1-C3 and H1-H3) hypertrophied cells and loss of intracellular spaces (*); D2, I2, and I3) starch accumulation; E1-E3 and J1-J3) accumulation of phenols (*); Epi ada = adaxial epidermis; Epi aba = abaxial epidermis; PP = palisade parenchyma; SP = spongy parenchyma; VB = vascular bundle.

As for hypertrophy, hypertrophied cells and thicker cell walls were observed following the initial dose of B, regardless of the source (Figures 2G1-3 and 2B1-3). In the most advanced stage of the lesions, disorganized palisade parenchyma and a reduction in intracellular spaces were observed (Figure 2B1).

Lesions began to appear on the leaves approximately on the 27 ^th day after the treatments were applied and symptoms were still observed up to the 80 ^th day. The borax source at the maximum dose (3 mg dm ^–3 ) caused the most pronounced symptoms of toxicity, followed by the dose of 1.5 mg dm ^–3 of the borax source and the doses of 3 mg dm ^–3 and 1.5 mg dm ^–3 of the ulexite source.

A gradient of symptoms is observed regardless of the B source. Initially, some punctual spots appear (Figure 3A). Later, in a more advanced stage, especially in plants submitted to the borax source (3 mg dm ^–3 ), the spots unite, forming a straw appearance on the margins of the leaves in the shape of an inverted V (Figure 3A). This symptom is like that of potassium deficiency (Marschner, 2012). The symptoms were observed exclusively in older leaves and no tissue necrosis was observed. Instead, the leaves exhibited a whitish appearance.

Figure 3
– Lesions on leaves of Khaya grandifoliola (C.) DC caused by B toxicity. A) Chlorosis on the edges of the leaves. Note that the lesions are whitish and distributed marginally and at the apex of the leaflets; B) Image obtained in a digital microscope. Note the necrosis of the lesion; C) Same lesion as in B observed under polarized light in a light microscope. Note the presence of crystalline structures at the edge of the lesion (arrow).

The symptoms occur in the venules (smaller vascular bundles) (Figure 3B), which are unloading regions of the xylem. This suggests that an excess of B unloading via the xylem could be the cause of the lesions. The evaluation of the lesion under polarized light in a light microscope revealed the accumulation of crystals on the lesion edge (Figure 3C), which may be Ca oxalate crystals due to the stress caused by B excess.

Discussion

Plants grown in the control treatment (without B) did not exhibit symptoms of leaf tissue deficiency (Figure 1A). The natural B content of the soil, even at a low concentration (0.2 mg dm ^–3 ), was sufficient for the plants to avoid symptoms of deficiency, such as wrinkling of the leaf blade. Nevertheless, this does not guarantee that the plant is not B deficient, as they may be marginally deficient (hidden hunger), a stage that is not observable with the naked eye, only through chemical analysis of the leaves (Marschner, 2012).

The plants were still in the initial stage of development. As it is a late secondary species, the visual symptoms of micronutrient deficiency are not commonly observed in the initial growth stage.

Boron is essential for the formation of cell walls, a crucial trait for noble-use forest species, as trees should have a straight trunk (Ribeiro et al., 2017). It is not uncommon to observe crooked plants in the field due to B deficiency (Silveira et al., 2000). In addition, B deficiency can result in paralysis, the death of the apical meristem, and the cessation of emission of lateral shoot formation. Therefore, it is crucial to maintain optimal levels of B in plants (Marschner, 2012).

Boron levels in the plant vary according to the species, leaf age, and its position in the crown. Higher levels are concentrated in the lower and older parts of the plant due to its low mobility in the phloem (Marschner, 2012). The literature still needs to classify adequate B levels for the genus African mahogany ( Khaya spp.). However, adequate B levels have been reported for other forest species, such as those of the genus of Eucalyptus . For eucalyptus, for example, the lower parts of the plant are considered adequate when the contents are close to 85 mg kg ^–1 , deficient when they are below 21 mg kg ^–1 , and toxic when they are above 360 mg kg ^–1 (Silveira et al., 2000). Consequently, it can be inferred that African mahogany exhibits a lower degree of tolerance to excess levels of B.

Boron plays a crucial role in the translocation of sugars (Marschner, 2012). Consequently, under conditions of low B availability, the plant may have trouble translocating starch to new parts (roots and leaves), resulting in B accumulation in old leaves, as observed in African mahogany. This accumulation has already been observed in other species, such as sugarcane, where plants cultivated with low B availability exhibited the lowest starch translocation and consequently the highest B accumulation (Crusciol et al., 2021).

Boron plays a direct role in the formation and stability of plant cell walls. It binds to pectin residues (rhamnogalacturonan type II (RG-II)) to form the primary cell wall, as described by Marschner (2012). It is estimated that more than 90 % of the total B in plant tissues is bound to cell walls (Matoh et al., 1992). This complexation occurs in the pectin fraction, which acts in cell wall cementation (Brown and Hu, 1993; Matsunaga and Nagata, 1995). This explains the increase in cell wall thickness observed in African mahogany. In coffee plants, Rosolem and Leite (2007) also observed that the B content in the cell wall increased in the proportion to the B concentration in the soil.

Different authors frequently discuss the formation of Ca oxalate in plants grown under heavy metal toxicity. (Mazen, 2004; Jáuregui-Zúñiga et al., 2005; Faheed et al., 2013). Nevertheless, there are no specific reports on the formation of Ca oxalate for B toxicity. The same authors propose that this accumulation represents a defense mechanism against toxicity and that a similar phenomenon may have occurred in plants grown with excess B.

It can be inferred that an excess of B causes more significant damage than a deficiency does in African mahogany during the early stages of development. Consequently, the use of smaller doses and sources of medium and low solubility is indicated during the initial stage of development of the seedlings. Subsequently, in the stages of top dressing, the application of higher doses is necessary to supply the demand for B throughout the cycle up to the point of high cycling of forest nutrients, which is a time when plants no longer respond to mineral fertilization. Finally, further studies should be conducted throughout the crop cycle to provide data that correlates B levels with wood quality and yield to increase the efficiency of using borate fertilizers.

Acknowledgments

The authors thanks to the Post-Graduate Program in Soils and Plant Nutrition of the Departamento de Ciências do Solo at the Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (USP/ESALQ). Besides, we thank the laboratory of electron microscopy ‘Prof. Elliot Watanabe Kitajima’ at the Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo (USP/ESALQ) for providing the infrastructure for the microscopy analysis

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Edited by

Edited by: José Lavres Júnior

Publication Dates

• Publication in this collection
  09 Sept 2024
• Date of issue
  2024

History

• Received
  25 July 2023
• Accepted
  09 Feb 2024