Structural variation among leaves in Aechmea distichantha Lem. (Bromeliaceae) rosettes, considering apical and basal differences

Highlights

• Anatomical features may define positive strategies for water acquisition and storage.

• The degree of methyl-esterification of pectins in bromeliad leaves, at different positions along the rosette, can maximize water storage.

• The water storage tissue has higher plasticity index than other leaf tissues at different positions along the rosette.

• Cell elongation and elasticity depend on the maintenance of HGAs with high methyl-esterified in water storage tissue.

Abstract

In tank-dependent bromeliads, leaves may exhibit anatomical and functional differences along the apical and basal regions, or according to the different positions in the rosette. Thus, the apical region of the leaf may invest in photosynthetic tissues, while the basal one invests in structures for water and nutrient storage. We suppose here, that differences among the tissue functions are strongly related to anatomical traits, especially the degree of methyl-esterification of pectins in the cell walls, at different positions along the rosette. Thus, the aims of this study were to quantify anatomical variations and describe the pectin composition of the cell wall, along the Aechmea distichantha Lem. rosette, to assess how the different tissues varied. We found that the water storage tissue showed higher variation between the apex and the base of the leaves than the other tissues, with higher expansion between the fourth leaf in development and the outer leaf in the rosette. Moreover, its cells were intensely labeled for epitopes of high methyl-esterified HGs, recognize by JIM7 antibody. The presence of pectin with high methyl-esterified groups in water storage tissue provides greater cell wall elasticity. The chlorenchyma showed the lowest Relative Distance Plasticity Index values, and its development in A. distichantha seems to occur early, in a very young leaf and inside the rosette tank.

Introduction

Among the Brazilian plant physiognomy, the campo rupestre vegetation stands out for the great diversity of species and remarkable heterogeneity of habitats (Conceição et al., 2007; Jacobi et al.,2007). In this habitat, rocky outcrops with low availability of nutrients and water determine a great diversity of xeromorphic species (Porembski, 2007), including tank-dependent bromeliads (Rapini et al., 2008; Takahashi and Mercier, 2011). The tanks are made up by densely overlapping leaf bases (rosette), where water and organic compounds are absorbed by absorptive foliar trichomes (peltate scales) and stored in specialized water storage tissues (Benzing, 1976, 2000; Givnish et al., 2014; Males and Griffiths, 2017; Popp et al., 2003; Schmidt and Zotz, 2001). The peltate scales are the most notable and adaptive feature in bromeliads and replace the water uptake role of the root system (Benzing, 1976, 2000; Tomlinson, 1969). In tank-dependent bromeliads, leaves may exhibit anatomical and functional differences along the apical and basal regions (Freschi et al., 2010) or according to different positions in the rosette, which should be determinant for bromeliad adaptation. In general, the apical region of the leaf invests in photosynthetic tissues, while the basal one invests in structures for water and nutrient storage (Freschi et al., 2010; Schmidt and Zotz, 2001). However, there are no studies that quantify the anatomical variations between the apex and the base of leaves at different positions in the rosette.

In addition to anatomical organization, the cell structure may define positive strategies for water acquisition and storage. During plant organ development or environmental condition variations, the cell walls are continually assembled, disassembled, and deformed (Caffall and Mohnen, 2009; Palin and Geitmann, 2012). The pectic constitution of the cell wall is dynamic, and functionally associated with primary tissue functions. Pectin is one of the most abundant components in cell wall matrix, constituting up to 35% of the primary walls of non-grass monocots (Jones et al., 1997; Mohnen, 2008). It is structurally and functionally the most complex polysaccharide (Palin and Geitmann, 2012), with a significant impact on the physico-chemical properties of the cell matrix (Mohnen, 2008). Pectins form a heterogeneous group of rich galacturonic acid polysaccharides (Cosgrove, 1997) that may occur in three main domains: rhamnogalacturonan I (RG-I), rhamnogalacturonan II (RG-II), and homogalacturonans (HGs) (Albersheim et al., 2011; Pérez et al., 2003; Ridley et al., 2001; Willats et al., 2001). HGs is the most abundant in the primary cell wall matrix of land plants (Ridley et al., 2001; Willats et al., 2001), representing 60% of the total pectins (Mohnen, 2008; O’Neill et al., 1990). They are synthesized in the high methyl-esterified form (Palin and Geitmann, 2012), and can be modified to the low methyl-esterified form during plant development (Xiao and Anderson, 2013). The process of methyl-esterification changes the functionality of pectins in the cell wall and, consequently, affects tissue function (Albersheim et al., 2011). However, few studies address the variation in cell wall pectin during leaf development, especially in monocots (Carpita, 1984, 1989; Yapo, 2010).

Differences in the degree of pectins methyl-esterification in bromeliad leaves, at different positions along the rosette, can maximize water storage in the water storage tissue. Herein, we investigated tissue variations, including immunocytochemical changes of the cell wall along the Aechmea distichantha Lem. rosette. Histometric variations and changes in cell wall composition, between the apex and base of leaves at different positions in the rosette, drive the major questions of this study: (a) Are there structural differences between proximal and distal leaves of bromeliad tanks? (b) Considering different positions along the A. distichantha rosette, and between apex and base positions, which leaf tissues are more plastic? (c) What is the magnitude of these differences?