morPho-anatomical featureS of the leaveS and StemS

of bacchariS notoSergila (aSteraceae) and their

relationShiP with the environment and chemical control

caracteríSticaS morfo-anatómicaS de laS hojaS y talloS de bacchariS

notoSergila (aSteraceae) y Su relación con el ambiente y control

químico

1

2

3

Alejandra V. Carbone , Federico E. Fernández , Marcelo P. Hernández

,

4

5

andAna M. Arambarri

Santiago M. Martínez Alonso

Summary

Background and aims: Baccharis notosergila is an aggressive weed inhabiting the

Salado river basin, Buenos Aires province, Argentina. The aims were: to analyze

the morpho-anatomy and histochemistry of aerial vegetative organs in order to

understand the adaptation strategies that ensure its survival, as well as to expand

knowledge on traits determining resistance to the control methods applied.

M&M: The material collected was prepared and examined with conventional techniques

of microscopy. Histochemical tests were performed.

Results: The major features found were small and deciduous leaves; uniseriate

epidermis with massive and striate cuticle; stomata at level or slightly above the other

epidermal cells and glandular trichomes secreting oily substances; stomata on both

surfaces and isobilateral mesophyll. Starch, phenolic and lipophilic substances, and

resins were identiﬁed in leaves and stems, and calcium oxalate crystals in leaves,

stems and capitate trichomes.

Conclusions: The aerial vegetative organs features of B. notosergila explain its

tolerance to the unfavorable conditions of the Salado river basin area, as well as

its competitive ability over others species of the natural prairie. The reduced and

deciduous leaves, the epidermal traits, and chemical substances found constitute a

physical and chemical barrier reducing dehydration as well as the penetration of the

herbicides applied for its control. Botanical knowledge of B. notosergila is the basis to

develop new and appropiate management methods for this species.

1

. Prof. Adjunta de Morfología

Vegetal, Facultad de Ciencias

Agrarias y Forestales (FCAyF),

Universidad Nacional de La Plata

(

UNLP), La Plata, Argentina.

Instituto de Fisiología Vegetal,

INFIVE-CONICET-UNLP)

. Forrajicultura y Praticultura,

FCAyF, UNLP

. Laboratorio de Morfología

Comparada de Espermatófitas

LAMCE). Sistemática Vegetal,

(

2

3

(

FCAyF, UNLP. Botánica Sistemática

II, DivisiónPlantas Vasculares,

Facultad de Ciencias Naturales y

Museo (FCNyM), UNLP

4

5

. Técnico (INFIVE-CONICET-UNLP)

. Prof. jubilada de Morfología

Vegetal, Investigadora FCAyF, UNLP

1

3

-5. FCAyF, UNLP, 60 y 119, C. C.

1 (1900) La Plata, Buenos Aires,

Key wordS

Argentina.

Aboveground system, environmental adaptation, stress tolerance.

*anaramba@gmail.com

reSumen

Citar este artículo

Introducción y objetivos: Baccharis notosergila es una maleza agresiva que habita

la Depresión del Salado, provincia Buenos Aires, Argentina. Los objetivos fueron:

analizar la morfo-anatomía e histoquímica de los órganos vegetativos aéreos para

entender las estrategias de adaptación que aseguran su sobrevivencia, así como

profundizar el conocimiento sobre los caracteres que determinan la resistencia a los

métodos de control.

CARBONE, A. V., F. E. FERNÁNDEZ,

M. P. HERNÁNDEZ, S. M. MARTÍNEZ

ALONSO &A. M. ARAMBARRI. 2021.

Morpho-anatomical features of

the leaves and stems of Baccharis

notosergila (Asteraceae) and their

relationship with the environment

and chemical control. Bol. Soc.

Argent. Bot. 56: 423-444.

M&M: El material recolectado fue preparado y analizado con técnicas convencionales

para microscopía. Se realizaron pruebas histoquímicas.

Resultados: Los principales caracteres encontrados fueron hojas pequeñas y

caedizas, anﬁstomáticas con mesoﬁlo isobilateral; epidermis uniseriada, cutícula

masiva y estriada, estomas a nivel o ligeramente elevados y tricomas glandulares

que secretan sustancias oleosas. Se identiﬁcaron sustancias lipofílicas y fenólicas,

almidón y resinas en hojas y tallos y se hallaron cristales de oxalato de calcio en

hojas, tallos y tricomas capitados.

DOI: https://doi.

org/10.31055/1851.2372.v56.

n4.33519

Conclusiones: Las características de los órganos vegetativos aéreos de B. notosergila

explican su tolerancia a las condiciones desfavorables del área de la Depresión del

Salado, así como su habilidad competitiva y predominancia sobre otras especies de

la pradera natural. Las hojas pequeñas y deciduas, sus características epidérmicas

y sustancias químicas encontradas constituyen una barrera física y química para

la deshidratación y penetración de los herbicidas aplicados para su control. El

conocimiento botánico de B. notosergila es la base para el desarrollo de nuevos y

apropiados métodos para el manejo de esta especie.

Recibido: 20 Jun 2021

Aceptado: 3 Set 2021

Publicado en línea: 4 Nov 2021

Publicado impreso: 20 Dic 2021

Editora: Ana María Gonzalez

PalabraS clave

Adaptación ambiental, sistema vegetativo aéreo, tolerancia al estrés.

ISSN versión impresa 0373-580X

ISSN versión on-line 1851-2372

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Bol. Soc. Argent. Bot. 56 (4) 2021

introduction

just been said, there is not a comprehensive study of

aboveground system of B. notosergila. Therefore,

The genus Baccharis L. is the richest in species the aims of this study were to investigate leaves

within the Astereae tribe, comprises from 354 and stems morphology, structure and histochemical

species (Müller, 2013) to 440 (Heiden et al., 2019) features to ascertain whether a correlation exists

of exclusively American distribution. Zuloaga et al. between the leaves and stems traits and survival

(2019) reported 210 species for southern cone of strategies, and to obtain some insight into the

South America (Argentina, southern Brazil, Chile, biological problems concerning the resistance to

Paraguay, and Uruguay). In Argentina inhabit current control methods.

9

9 species (Giuliano & Plos, 2014). The present

contribution is about Baccharis notosergila Griseb.,

which is a woody shrub that inhabit in the Salado materialS and methodS

river basin situated in Buenos Aires province

(Argentina). This region alternate cyclically periods Plant materials

of drought and ﬂoods, the land surface is nearly Plants of B. notosergila having fully developed

horizontal with predominance of saline-alkaline leaves were collected during the spring of 2018-

soils and a deﬁcient drainage. This area is occupied 2020 in the “El Amanecer” establishment-

by natural pastures and principally dedicated to farm situated at 57º37’ W, 35º15’S in Vieytes,

livestock farming (Rodriguez & Jacobo, 2012). Magdalena party (Pdo.), Buenos Aires province

Baccharis notosergila not only reduce with its (Prov.), Argentina. The botanical material was

cover the area accessible to grazing, but produce identiﬁed and the vouchers were deposited in the

strong competition for water, nutrients and light herbarium of Facultad de Agronomía, Universidad

with the species of value of the natural grassland, Nacional de La Plata, and registered as: 17-

generating a process of degradation that normally XII-2018, F. Fernández & A. Carbone 1, 2, 3, 4

result in low productivity (Sione et al., 2006). (LPAG); F. Fernández & A. Carbone 5, 15-X-2019,

Baccharis notosergila in the Salado river basin has (LPAG); F. Fernández & A. Carbone 6 (specimen

shown to be resistant to mechanical and chemical from half hill), 7 (specimen from alkaline-saline

control (Urdampilleta, 2019; Carbone et al., 2019). lowland), 8 (specimen from sweet lowland), 11-

For the reasons mentioned above, this species XI-2020 (LPAG). In addition, specimens having

is included in the project on problematic weeds, leaves from Instituto de Botánica Darwinion were

developed in the Facultad de Ciencias Agrarias consulted. ARGENTINA. Prov. Buenos Aires: Pdo.

y Forestales, Universidad Nacional de La Plata Berazategui, Hudson, 16-IV-1927, Burkart 1302

(Argentina). In a previous paper, Carbone et al. (SI) (image 15). Prov. Entre Ríos: Dpto. Concordia,

(2019) analyzed the underground system in which 31-I-1927, Burkart 1122 (SI), Det. Cabrera (image

was found a xylopodium with buds constituting 14). Dpto. Gualeguaychú, 10-IV-1960, Burkart

a bud bank, either was detected in the radical 21988 & Gamerro (SI).

system the accumulation of inulin as the principal

reserve. According to Hayashi & Appezzato-da- Optical microscopy

Glória (2007) and Appezzatto-da-Glória & Cury

For anatomy study, mature leaves and stem

(2011), the presence of these two traits allow for fragments of diﬀerent specimens were ﬁxed in FAA

regeneration and survival through unfavourable (a solution of formaldehyde, glacial acetic acid, and

environmental conditions. Carbone et al. (2019), 70% ethyl alcohol, Johansen, 1940), then stored in

attributed to subterranean system’s traits the 70% ethanol. To analyze epidermis in surface view,

capacity to sprout and develop new organs in the the leaves were diaphanized using the method of

spring after mechanical and chemical control, and Franklin (1945) modiﬁed, for that, the leaves were

the accumulation of inulin reinforces the resprout boiled in ethyl alcohol 96º for 20 min, allowed to

and persistence of this shrub. Now, two questions cool were washed and bleached in 50% sodium

arise: what is the role of aerial vegetative organs in hypochlorite (NaClO) for 2 h, washed twice and

the survival of this species?, and what is its reaction submerged in a solution of hydrogen peroxide +

to the chemical control treatment?. Despite what has glacial acetic acid (1: 1 v/v) for 48 h, washed twice

424

A. V. Carbone et al. - Baccharis notosergila: aerial vegetative organs and environment

in distilled water, bleached again in 50% NaClO. & Chalk (1988) was followed in this work. The

At the completion of the bleaching process, ﬁve stomata types were recognized using the manual

washes in distilled water were carried out to remove of Ash et al. (1999). Trichomes were described

the NaClO, and samples were then transferred into considering the literary works (Ramayya, 1962;

a solution of chloral hydrate (5%) for 24-48 h. To Freire et al., 2007; Tosoratto et al., 2016, and Budel

complete the process, some leaves were washed et al., 2018).

and stained with safranin or Oil red “O”, on others

was applied the peeling method to obtain the Scanning electron microscopy (SEM)

epidermis which were also stained. To analyze

It was performed using portions of stem and

the structures, freehand cross-sections of stems, leaf blade. They were taken from ﬁxed material,

petiole and at leaf blade middle part of leaves were dehydrated in ethyl alcohol (100º) for 24 h. Then

cut; the selected sections were bleached in 50% the samples were aﬃxed on stubs by double-sided

NaClO, washed thrice with distilled water, then adhesive tape and were submitted to metallization

a successive double staining was performed with with a ﬁne and thin gold layer. Afterwards they

Alcian blue and safranin (Luque et al., 1996), on were examined with a Philips 505 SEM, and

others a metachromatic staining was performed micrographs were prepared. Center for Research

using Toluidine blue “O” (0.05%) (O’Brien et al., and Development in Applied Sciences “Dr. Jorge

1

964) or Cresyl brilliant blue (0.05%) (Pérez & J. Ronco” (CINDECA), National Council for

Tomasi, 2002), and also a monochromatic staining Scientiﬁc and Technical Research (CONICET),

was made using alcoholic solution of safranin National University of La Plata (UNLP).

(

80%) (D’Ambrogio, 1986). The sections, clariﬁed

leaves, and epidermis were mounted in gelatin-

glycerin on glass slides and sealed with nail polish. reSultS

The histochemical analysis was performed on

freehand sections of leaf and stem samples. To Leaf morphology

test lipophilic substances an alcoholic solution of

Leaves are deciduous and have an alternate

Oil red “O” was used (Gurr, 1971), the red color arrangement. They are variable in shape and size.

indicated positive test. Detection of phenolic They are elliptic or elliptic-obovate, linear-elliptic

compounds (tannins) was performed using ferric and linear. The largest elliptic or elliptic-obovate

chloride (10%) and sodium carbonate (2%) frequently are situated in the basal part of the plant

(

Zarlavsky, 2014), a green-blue color was a or stems, the linear-elliptic towards the middle part,

positive test. Starch was identiﬁed with Iodine- and the linear leaves at the top of the stem or the

Potassium-Iodide (IKI) (Ruzin, 1999) a black-blue upper branches of the plant. All leaves have acute-

color indicate positive test. Resins were detected mucronate apex, decurrent base with petiole, and

using a saturated solution of copper sulphate (Cosa reticulate vascularization. The largest leaves have

et al., 2014) a color emerald green indicate positive the serrate margins with 1-4(-10) teeth on each

test. Additionally, toluidine blue “O” was used to margin; 3.7-7 cm long and 0.5-1 cm wide. The

contrast polyphenols (Tapia-Torres et al., 2014), a median leaves have a few teeth or entire margins,

color turquoise green was a positive test.

2.3-4.2 cm in length and 0.3-0.5 cm in width, and

The leaf morphology and phyllotaxy type the smallest linear leaves have entire margins,

were evaluated through a visual inspection. To measuring 1-2.5 cm long x 0.1-0.3 cm wide (Fig. 1).

see details a Bausch & Lomb stereomicroscope

was used. Photographs were taken with a digital Epidermal tissue in surface view by SEM

camera, resolution 12 MP. Slides were analyzed

The leaves epidermis exhibit striate and massive

with a Nikon E200 LED optical microscope cuticle and frequently waxes overlap the guard

and using micrometrics SE Premium software. cells, partly obscuring them (Fig. 2A). Stem

The measurements of outer periclinal epidermal topography view by SEM reveals longitudinal ribs

cell walls and cuticle thickness in micrometers alternating with grooves, all covered by striate

(

µm) were obtained by using ImageJ software cuticle, and the stomata located in the depth of the

González, 2018). Terminology used by Metcalfe grooves (Figs. 2 B; 8B).

425

Bol. Soc. Argent. Bot. 56 (4) 2021

and less frequently anisocytic. Each stoma shows

in surface view the outer stomatal ledge, a polar

thickening, and ellipsoidal stomatal aperture (pore)

(

Fig. 3A-E). The trichomes are found on both

leaf blade surfaces, margins, and the petiole. The

trichomes types are: (i) Biseriate capitate glandular

with 2 basal cells and 6-8 cells which contains druses

(Fig. 4A); (ii) Bulbiferous ﬂagelliform glandular

(bfg) type II, uniseriate and curved body with 3-7

(frequently 4) rounded cells, the terminal swollen

spherical, and a translucent ﬂagellum-like apical cell

Fig. 4B), less frequently are found bfg type I with

straight body of 5-7(-8) cells and ﬂagellum cell (Fig.

D); (iii) Uniseriate capitate glandular trichome

(

4

composed by one basal cell, 2-6(-8) stalk cells and

a multicellular head (Fig. 4C). All the trichomes

have basal cells cutinized, given positive reaction

for lipophilic compounds, and are responsible for

the secretion of oil droplets deposited over the leaf

blade surface (Fig. 4D-F). The biseriate glandular

trichomes can be seen forming a tuft themselves

(Fig. 4A), but frequently appear clustered with bfg

trichomes (Fig. 4B, D-G) in tufts and localized

in a small epidermal depression. Either of the bfg

trichomes can occur singly. It was observed that

frequently two or three tufts appear connected

by more elongated epidermal cells with cuticular

thickened over the anticlinal cell walls (Fig. 4G).

Fig. 1. Leaf morphology. It shows the variability of B.

notosergila leaf size and shapes. The large elliptic The uniseriate capitate trichomes are found in lower

and elliptic-obovate leaves (3.7-7 cm length); with frequency and solitaries (Fig. 4C).

toothed margins, and it may be seen the reticulate

venation. The median elliptic and linear-elliptic

leaves (2.3-4.2 cm length), with toothed or entire

margins. The small linear leaves (1-2.5 cm length),

with entire margins. Scale: 2 cm.

The caulinar axis exhibits epidermal cells

tangentially elongated on the ribs with slightly thick

anticlinal cell walls, and the surface covered by

waxes; in the grooves there are numerous actinocytic

stomata and trichome tufts (Figs. 3F; 4B).

Leaf structure

The petiole cross section next to attach the stem

Epidermal tissue in surface view by light microscope (basal part) shows a concave adaxial side forming

The epidermal cells on both leaf blade faces two lobes (Fig. 5A). This cross-section exhibits

are polygonal with anticlinal cell walls straight to quadrangular or rectangular epidermal cells,

slightly wavy, and the cuticle is striated especially covered by cuticle. The angular collenchyma occurs

around the trichomes and stomata. Generally, the in each lobe and some layers are found at middle

anticlinal cell walls are thin. Stomata are uniformly vein level. The parenchyma is composed by rounded

distributed over whole petiole and leaf blade cells except the chlorenchyma which is formed by

surfaces and on the margins. They are randomly palisade parenchyma on the abaxial side, except at

distributed, however, the stomata longitudinal axis is middle vein level. There are three main vascular

oriented following the longitudinal axis of the organ bundles and some traces. The cross section in the

(Fig. 2A). Stomata are predominantly actinocytic, middle part of the petiole length (Fig. 5B), exhibits

anomocytic, anomotetracytic, cyclocytic types a reduction of adaxial concavity; the collenchyma

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A. V. Carbone et al. - Baccharis notosergila: aerial vegetative organs and environment

Fig. 2. Leaf and stem surface view by SEM. A: Leaf epidermis with massive cuticle and waxes over the

stomata. B: Stem showing ribs and grooves covered by striate cuticle. Scales= A: 50 µm; B: 5 µm.

appears as one continuous subepidermal layer, (Fig. 6D). In the center, there are 3-4 layers of

increasing the layers at midvein level, and the colorless dense spongy parenchyma (Fig. 6C). The

chlorenchyma begin to extend to adaxial side. The vascular system is composed by collateral vascular

petiole cross section at the base of leaf blade (distal bundles each surrounded by a parenchyma sheath,

part, Fig. 5C), shows deltoid outline, however and cross the spongy parenchyma (Fig. 6C). The

at midvein level there are adaxial and abaxial xylem always is to the upper side. The middle

prominences, and the palisade chlorenchyma is vein exhibits in the center one collateral vascular

present on both sides except at middle vein level; bundle with ﬁber cap adjoining the xylem and

the wings of the leaf blade begin to appear. Along one to three secretory ducts next to phloem, all

the entire length of the petiole there are three main surrounded by a parenchyma sheath adding several

vascular bundles. Each vascular bundle has ﬁber layers of thin-walled parenchyma cells that connect

caps on the xylem and phloem sides, and one to with two or three layers of angular collenchyma

three secretory ducts next to phloem ﬁber cap, all below the epidermis, on both sides (Fig. 6E). The

surrounded by a parenchyma sheath (Fig. 5D).

schizogenous secretory ducts exhibits a single

The leaf blade cross section exhibits the layered epithelium composed of 4-6 cells (Fig. 6D-

uniseriate epidermis formed by quadrangular E). In all materials analyzed the linear-elliptic and

or rectangular epidermal cells with periclinal linear leaves have ﬁber cap only on the xylem side,

cell walls thin or conspicuously thicker, always and they have ample ducts, while in the largest

covered by a thin and striate cuticle (Fig. 6A, B). elliptic or elliptic-obovate leaves the vascular

The stomata are localized above or at level with the bundles have ﬁber caps on xylem and phloem

surrounding epidermal cells, and the guard cells sides (similar occurs in the petiole), and the duct

show conspicuous outer and inner stomatal ledges exhibit a reduced size (Fig. 6F). The teeth found on

(

Fig 6A, B). Internally the isobilateral mesophyll apex and margins of the leaves present hydathode

shows 2-3 layers of palisade parenchyma on structure, each tooth shows three vascular bundles

both faces interrupted at middle vein level, but which converge approaching the tooth end, the

continuous in the margins (Fig. 6C), sometimes epithema is poorly developed and there is an open

separated from the epidermis by collenchyma stoma at the tooth apex.

427

Bol. Soc. Argent. Bot. 56 (4) 2021

Fig. 3. Leaf and stem surface view by light microscope. A-E: Leaf. A: Anomocytic stoma, it exhibits the outer

stomata ledge and polar thickening; cuticular striaes are notable on subsidiary cells. B: Two actinocytic

stomata. C: Anisocytic. D: Anomocytic stoma on the left and anomotetracytic on the right. E: Ciclocytic. F:

Epidermis of stem in surface view showing rectangular epidermal cells with anticlinal cell walls straight and

thickened; epicuticular waxes visible as points on the surface, and an actinocytic stoma. Abbreviations= esa:

ellipsoidal stomata aperture; ew: epicuticular waxes; pt: polar thickening; osl: outer stomata ledge. Staining=

A, B, E, F: oil red “O”; C: safranin; D: toluidine blue “O”. Scales= A-F: 100 µm.

428

A. V. Carbone et al. - Baccharis notosergila: aerial vegetative organs and environment

Fig. 4. Trichome features. A: A tuft with two biseriate capitates glandular trichomes showing druses in cells.

B: A tuft showing three biseriate capitate trichomes clustered with three bulbiferous ﬂagelliform glandular

(bfg) type II (arrows). C: Uniseriate capitate trichome, solitary, rarely was seen in large leaves. D: A tuft

showing biseriate capitate trichomes clustered with bfg type II, and one bfg type I (straight) with numerous

oil droplets inner the trichome cells (arrows). E: A tuft showing the secretion of oil droplets and deposited

on the epidermal cells surface. F: A tuft exhibiting oil droplets in the ﬂagellum cell. G: Two tufts connected

by elongated epidermal cells with cuticular thickened on the anticlinal epidermal cell walls. Abbreviations=

bfgI: bulbiferous ﬂagelliform glandular straight (type I); bfgII: bfg curved (type II); cu: cuticle; dr: druses;

fc: ﬂagellum cell; hd: head; od; oil droplets; st: stalk cells; tf: tuft. Staining= A-E: safranin; F, G: oil red “O”.

Scales: A-G= 100 µm.

429

Bol. Soc. Argent. Bot. 56 (4) 2021

Fig. 5. Petiole cross section (CS). A: The CS near the insertion point on the stem is bilobed with

chlorenchyma on abaxial side except at middle vein; there are three main vascular bundles. B: The CS in

middle of the petiole length shows a reduction of lobes. C: The CS at base of the leaf-blade has a deltoid

outline beginning to develop the wings of the leaf-blade with chlorenchyma on both faces, except at middle

vein. D: detail of one vascular bundle showing caps of ﬁbers on the xylem and phloem sides, and on the

phloem side one duct; all surrounded by the parenchyma sheath. Abbreviations= abf: abaxial face; adf:

adaxial face; ch: chlorenchyma; fb: ﬁbers; lb: lobe; mv: middle vein; ph, phloem; ps: parenchyma sheath; re:

resins; xy, xylem. Scales= A-C: 300 µm; D: 100 µm.

The histochemical tests showed that some Comparing leaves structures collected from plants

epidermal cells are filled with tanniniferous inhabiting on half hill, alkaline-saline lowland and

substances, the guard cells of stomata also contain sweet lowland in the studied area

tannins and starch, and these compounds are

The leaves from half hill exhibit in surface view,

abundant in the mesophyll (Fig. 7A, B). In the thickened anticlinal epidermal cell walls, and striated

mesophyll, especially in the palisade parenchyma cuticle; on the teeth the epidermal cells shows thicker

cells there are many chloroplasts, oil bodies (Fig. cell walls. In cross section both epidermis, adaxial

6

B), and small prismatic crystals (Fig. 7C). In and abaxial, show conspicuous cellulosic thicker

the epithelial cells of ducts were identiﬁed oil on the cell walls; in the periclinal epidermal cell

droplets of volatile oils (Fig. 6E) and in the cavity walls the thickness ranged between 5.6-20.6 µm

were obtained positive reactions for resins and with a mean value of 14.2 µm (Fig. 6B). The leaves

polyphenols (Fig. 7D).

from alkaline-saline soils and from sweet lowland

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A. V. Carbone et al. - Baccharis notosergila: aerial vegetative organs and environment

Fig. 6. Leaf blade cross section (CS). A: epidermal cells with thin cell walls and thin cuticle, the stomata

slightly above the other epidermal cells, and the stoma guard cells with the cuticle forming conspicuous

stomatal ledges. B: epidermal cells with thick periclinal cell walls, thin and striate cuticle, and stomata guard

cells at level. Also may be seen the oil bodies in the mesophyll. C: Leaf-blade CS showing the prominences

at middle vein level, the uniseriate epidermis, stomata and trichomes on sides, isobilateral mesophyll

and vascular bundles (vb) across the spongy parenchyma. D: a detail of the obtuse margins showing the

palisade parenchyma continuous, separated from epidermis by some collenchyma cells; and marginal

vascular bundles, one with an ample duct. E: middle vein CS of a linear-elliptic leaf showing the collateral vb

with ﬁbers on the xylem side and two ample ducts on the phloem side containing volatile oils in the epithelial

cells, all surrounded by a parenchyma sheath and its extension towards the angular collenchyma cells.

F: middle vein CS of an large elliptic-obovate leaf showing the collateral vb with ﬁbers on both sides and

one reduced duct on the phloem side, all surrounded by a parenchyma sheath and its extension to under

epidermal collenchyma tissue. Abbreviations= co: collenchyma cells; dc: duct; ec: epithelial cells; fb: ﬁbers;

gc: guard cells; isl: inner stomatal ledge; ob: oil bodies; osl: outer stomatal ledge; pcw: periclinal cell walls;

ph: phloem; pp: palisade parenchyma; ps: parenchyma sheath; sp: spongy parenchyma; st: stomata; tsc:

thin and striate cuticle; vb: vascular bundle; xy: xylem. Scales: A, B, D-F: 100 µm; C: 500 µm.

431

Bol. Soc. Argent. Bot. 56 (4) 2021

Fig. 7. Leaf histochemical tests and crystals. A: Leaf blade cross-section (CS) showing presence of tannins

in epidermal cells, guard cells and mesophyll cells (test FeCl3). B: leaf blade CS showing starch grains in

mesophyll cells (test IKI). C: Leaf blade CS showing thin and striate cuticle (test oil red “O”); small crystals

in parenchyma cells (arrows). D: Vascular bundle showing two secretory ducts containing polyphenols

and resins (tests toluidina blue “O” and copper sulphate have been made). Abbreviations= cr: crystals; ep:

epidermis; gc: guard cells; me: mesophyll; ph: phloem; po: polyphenols; re: resins; sc: striate cuticle; st:

starch grains; ta: tannins; xy: xylem. Scales= A-D: 100 µm.

show in surface view, thin anticlinal epidermal cell cells (Fig. 6A) while in the leaves from half hill they

walls, and slightly striated cuticle. In cross section, appeared localized at level (Fig. 6B). The leaves

the periclinal epidermal cell walls thickness ranged from half hill shows the palisade parenchyma with

between 0.9-3.6 µm with a mean value of 2.3 µm abundant oil bodies (Fig. 6B), compared to leaves

and 1.7 µm, respectively (Fig. 6A). The cuticle in from alkaline-saline and sweet lowland.

all leaves is thin (0.4-2.7 µm) with a mean value of

1

.2-1.6 µm (Fig. 6A, B). The stomata in the leaves Stem structure

from alkaline-saline and sweet lowland are localized A young stem of 1-2 mm diameter, in cross-

somewhat elevated above to the other epidermal section, reveals a wavy outline with eight ribs

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A. V. Carbone et al. - Baccharis notosergila: aerial vegetative organs and environment

Fig. 8. Stem outline (1-2 mm diam.) and tissues in cross section. A: stem outline showing eight lobes or

ribs. B: Stem tissues: ch, chlorenchyma; co, collenchyma; en, endodermis; ep, epidermis; fb, ﬁber clusters;

ft, foliar trace; ph, secondary phloem; phf, secondary phloem ﬁbers; pt: pith; dc, duct; st, stomata; xy,

secondary xylem. Scales= A: 1mm; B: 400 µm.

and alternating grooves (Fig. 8A). The epidermis the cortex, a few vascular bundles corresponding

is unilayered and consists of quadrangular or to foliar traces are present. They each contain

rectangular cells. The external periclinal walls of xylem internally and phloem externally with a cap

the cells are thick and impregnated with lipids and of phloem ﬁbers and a secretory duct adjacent to

are covered by a cuticle of 1.2-3 µm thick. Stomata the ﬁbers. The vascular bundle is surrounded by

are localized in the grooves and are elevated a parenchyma sheath with cell walls impregnated

above the adjacent epidermal cells (Fig. 8B). with lipophilic substances. The endodermis is

In the outer cortex, two to six layers of angular formed by rectangular cells with thin cell walls

collenchyma are present beneath the ribs. Between impregnated with suberin, obscuring the Casparian

the collenchyma, three to four layers of palisade strips. In the vascular cylinder, ﬁber clusters are

chlorenchyma occur in the grooves. The inner found adjoining the phloem, and also ﬁbers are in

cortex comprises two or three layers of polygonal the secondary phloem. The secretory ducts with a

parenchyma cells, and the innermost layer is the uniseriate epithelium formed by 4-10 cells occur

endodermis surrounding the vascular cylinder. In in front of the phloem. The secondary xylem has

433

Bol. Soc. Argent. Bot. 56 (4) 2021

Fig. 9. Stem (3-4 mm diam.) in cross section. A: secondary bark (periderm) developed under the epidermis;

cork cells contain tannins (test ClFe3). B: This photograph shows cutin in the epidermis; lipophilic

substances in cork cell walls and in the endodermis cell walls (test oil red “O”); in the cortex may be seen

isodiametric parenchyma cells. C: Secondary phloem with ﬁbers and starch grains (test IKI). D: pith with

crystals. Abbreviations= ck: cork; cp: cortical parenchyma; en: endodermis; ep: epidermis; fb: ﬁber cluster;

ls: lipophilic substances; pe: periderm; phf: ﬁbers in the secondary phloem; pt: pith; st: starch grains; sty:

styloids; ta: tannins. Scales= A-D: 100 µm.

ﬁbers as the predominant component and tannins contain tannins (Fig. 9A). The cork cell walls are

are occasionally found in the secondary xylem. impregnated by suberin (Fig. 9B). In the cortex,

The center of the stem is ﬁlled with the pith the cortical parenchyma exhibits rounded cells,

formed by thin-walled parenchyma cells. In the and the most inner cell layer, the endodermis,

perimedullary cells, calcium oxalate crystals are also shows cell walls impregnated with lipophilic

observed (Fig. 8B).

substances (Fig. 9B). Internally, the parenchyma

A caulinar axis of 3-4 mm diameter exhibits of the secondary phloem contains starch grains

rounded outline and similar structure as was (Fig. 9C). In the medullary rays and pith there are

described above, however the periderm (cork abundant crystals which have very thin tabular

+

cork cambium + phelloderm) is developed shape that according to the focal distance may be

below the epidermis (Fig. 9A, B). The cork cells confused with raphides (Fig. 9D).

434

A. V. Carbone et al. - Baccharis notosergila: aerial vegetative organs and environment

diScuSSion

The epidermal cells and cuticle features may be

attributed to environmental factors. Roth (1984),

Leaf morphology. The leaves arrangement and reported that when the foliar epidermis is exposed

features found in B. notosergila accord well greater luminosity and reduced humidity develop

with description of Baccharis leaves reported by characters of the “sun leaves”, such as the straight

Heiden et al. (2009). The petiole is not common epidermal anticlinal cell walls. Nughes et al. (2013)

in Baccharis leaves, however it has been found in found the principal factor producing the “sun

several species (e. g., Souza et al., 2011; Jasinski et leaves” is the high light intensity, whereas they

al., 2014; Bobek et al., 2016; Tosoratto et al., 2016). suggested the humidity is related to the stomata

Respect to the variability of leaf margins dentate or number and size. In B. notosergila, the linear leaves

entire, is common trait for the genus (Budel & predominantly found in the high part of the plants,

Duarte, 2008; Oliveira et al., 2011; Souza et al., show the most reduced size and present epidermal

2

011). Baccharis notosergila has leaves generally anticlinal cell walls slightly thickened, also the

with reduced foliar expansion and stay on the plant epidermal periclinal cell walls conspicuously

about ﬁve months in spring and beginning summer. thickened were found in elliptic-obovate leaves

This is the best period to do photosynthesis. The collected in half hill. These features may be

character deciduous of the leaves is a favorable adaptations to more exposed localization to weather

feature to the economy of water without aﬀect factors such as wind, high light intensity, because

its physiology, because it can continuous doing straight and thick periclinal cell walls tend to

photosynthesis with its numerous younger green decrease the excessive loss of water (Fahn & Cutler,

stems which have active palisade chlorenchyma. It 1992), and prevent cell collapse due to dehydration

would be an adaptation to the environment (Roth, (Cosa & Dottori, 2010). The striated cuticle would

1

984). On the other hand, the deciduous, small and be a response to the environment as prevent rapid

narrow leaves would be unfavorable to penetration dehydration (Fahn & Cutler, 1992). The massive

of herbicide treatments.

aspect found in the cuticle would be produce by

waxes deposited over the cuticle (Barthlott et

Hydathodes. Teeth found in leaves are al., 1998). Cuticle and epicuticular waxes also

hydathodes. The structure has been found in constitute the outermost defensive barrier of plant

Asteraceae and in some species of Baccharis leaves against pathogens because their repellents

(

Smiljanic, 1969; Lersten & Curtis, 1985). The properties (Barthlott et al., 1998; Stenglein et al.,

function is to discharge water (guttation), however, 2005). In cross sections the cuticle was found thin,

it would be interesting to do a more comprehensive however the chemical composition of the cuticle

study about the structure and function in B. is of a great importance limiting transpiration,

notosergila.

and thin cuticles are often eﬀective in preventing

excessive cuticular transpiration (Merida et al.,

Epidermal cells and cuticle. The polygonal 1981). The chemical weed control is more diﬃcult

epidermal cell shapes in surface view found in in those species which have less foliar area and

Baccharis notosergila accords well with the genus thicker cuticle and epicuticular waxes (Westwood

pattern (Ariza Espinar, 1973), while the anticlinal et al., 1997; Dall’Armellina & Zimdahl, 1989;

cell walls straight to slightly wavy also have been Carbone, 2015), whereas a thin cuticle could be

reported for some species (Cortadi et al., 1999; an advantage for the penetration of the herbicide,

Freire et al., 2007; Budel & Duarte, 2008; Oliveira and therefore, increase its absorption into the inner

et al., 2011; Souza et al., 2011; Bobek et al., 2015). tissues (Santier & Chamel, 1992), however in this

The cuticle of B. notosergila in surface view appears case the epicuticular waxes and volatile oils over

massive and striated in leaves and stems, but it is the leaves and stem surfaces could be a barrier

always thin. These cuticle traits coincide with the to penetration the herbicides or phytosanitary

most cases reported in the literature (Ariza Espinar, treatments applied.

1

&

2

973; Cortadi et al., 1999; Budel et al., 2003; Budel

Duarte, 2007; Petenatti et al., 2007; Jasinski et al.,

014; Bobek et al., 2015, 2016; Budel et al., 2018).

Stomata types. Actinocytic, anisocytic,

anomocytic, anomo-tetracytic and cyclocytic types

435

Bol. Soc. Argent. Bot. 56 (4) 2021

of stomata were found in B. notosergila. According environment with high solar radiation and also

to Metcalfe & Chalk (1950), the Asteraceae family it would be a manner to increase photosintetic

may present anomocytic and anisocytic stomata, process, because increase gas exchange proving

being the former predominant. These two types more eﬃcient when compared to hypostomatic

have been also reported in the genus by Ariza leaves (Roth, 1984; Parkhurst, 1978; Arambarri

Espinar (1973), and were described for most et al., 2011; Carbone, 2015). Liesenfeld et al.

species of Baccharis (Cortadi et al., 1999; Budel (2019), analyzed morphology and anatomy traits

et al., 2004; Budel & Duarte 2007, 2008, 2010; of leaves in 34 species of Asteraceae inhabiting in

Petenatti et al. 2007; Souza et al., 2011; Tosoratto extreme environmental conditions, and they also

et al., 2016). However, cyclocytic was previously reported among the characteristics adaptive to xeric

referred for B. notosergila (Freire et al., 2005, environments, the amphistomatic leaves.

2

007), and several authors mentioned tetracytic

type (e. g., Freire et al. 2007; Bobek et al., 2015,

016; Budel et al., 2018; Ornellas et al., 2019). The in B. notosergila has been reported for many

Mesophyll. The isobilateral mesophyll found

2

actinocytic stomata type was mentioned by Freire et Baccharis species (e. g., Oliveira & Bastos, 1998;

al. (2007) for 11 species of Baccharis, and Pereira Budel & Duarte, 2007, 2008, 2010; Petenatti et

et al. (2014) for B. milleﬂora DC. On the other al., 2007; Jasinski et al., 2014; Barreto et al.,

hand, diﬀerent stomata types in the same epidermis 2015; Bobek et al., 2015, 2016; Tosoratto et al.,

of one species of Baccharis have been previously 2016; Budel et al., 2018). Metcalfe & Chalk

encountered (Pereira et al.; 2014; Budel et al., (1950) noted the relationships among presence

2

015; Bobek et al., 2015, 2016; Budel et al., 2018; of adaxial stomata in plants with isobilateral

Ornellas et al., 2019).

organization of palisade mesophyll. The correlation

among amphistomatic leaves and isobilateral

Stomata distribution. Baccharis notosergila mesophyll was also found by Arambarri et al.

presents amphistomaty, and the stomata localized (2011). Nughes et al. (2013) studied the behavior

at level or elevated above the epidermal cells of Celtis ehrenbergiana (Klotzsch) Liebm., plants

around them. Both stomata characteristics have growing under temperate and wet weather with

been reported in Baccharis by diﬀerent authors available water, and the leaves exposed to a high

(

2

Metcalfe & Chalk, 1950; Budel et al., 2003, light intensity were amphistomatic with isobilateral

004; Budel & Duarte 2007, 2008, 2010; Petenatti or homogeneous (palisade parenchyma) mesophyll,

et al., 2007; Jasinski et al., 2014; Bobek et al., whereas the leaves expanded under low light

015, 2016; Ornellas et al., 2019). Metcalfe & intensity were hypostomatic with dorsiventral

2

Chalk (1950) demonstrated that a significant mesophyll. Ornellas et al. (2019) had similar results

number of plant species have amphistomatic studying six species of Baccharis inhabiting in the

leaves. Mott et al. (1982) suggested that the high-altitude grasslands, they found the occurrence

presence of stomata on both sides of the leaf has of stomata and the mesophyll organization seem to

an adaptive signiﬁcance, being a derived character be correlated, the amphistomatic leaves tend to be

and ecologically correlated with the increased leaf isobilateral.

conductance of carbon dioxide in plants living

in open areas and full sun environments or with

Trichomes. Glandular trichomes were found

high light intensity, with seasonal variations of in aerial vegetative organs of B. notosergila:

water availability in the soil. Mott & Michaelson (i) Biseriate capitate glandular, (ii) Bulbiferous

(1991) established that high light intensity produce ﬂagelliform glandular type II, and rarely type I,

amphistomatic leaves in Ambrosia cordifolia (A. that accords well with description provided by

Gray) W. W. Payne (Asteraceae), and increase leaf Tosoratto et al. (2016) and Budel et al. (2018),

thickness, photosynthetic capacity, and maximum and (iii) Uniseriate capitate glandular which was

stomatal conductance, because the presence of previously reported by Petenatti et al. (2007)

stomata on adaxial and abaxial sides would be for B. sagittalis (Less.) DC. and B. triangularis

reducing diﬀusional limitations to photosynthesis. Hauman. The biseriate capitate and ﬂagelliform

Amphistomatic leaves are common of arid trichomes have been found in nearly all Baccharis

436

A. V. Carbone et al. - Baccharis notosergila: aerial vegetative organs and environment

species. They have been cited for the genus by

Fibers and endodermis. Baccharis notosergila

Ariza Espinar (1973) who namely “pilose nests”, showed scarce fibers in the leaves, frequently

and have been reported for B. notosergila by reduced to xylem side in the vascular bundles.

Freire et al. (2007) and Heiden et al. (2009), and However, they were abundant in the secondary

in other species of Baccharis (e. g., Cortadi et xylem of the stem. Also, the stem showed the

al., 1999; Budel & Duarte, 2007, 2008; Budel et endodermis with Casparian strips surrounding the

al., 2003, 2004, 2012, 2015, 2018; Freire et al., vascular system. These stem characteristics were

2

005; Petenatti et al., 2007; Souza et al., 2011; also found by Tosorato et al. (2016) in B. salicifolia

Jasinski et al., 2014; Pereira et al., 2014; Barreto Nutt. According to Fahn & Cutler (1992) the

et al., 2015; Bobek et al., 2015, 2016). For many presence of ﬁbers and endodermis are xeromorphic

years, the ﬂagelliform trichomes were described traits with the function to protect tissues of the

as non-glandular trichome multicellular with a dehydration.

whip-like apical cell with diﬀerent characteristics

(

e. g., Ramayya, 1962; Ariza Espinar, 1973; Freire

Oil bodies. These lipid bodies were identiﬁed

et al., 2007). However, Budel et al. (2012, 2015) in the leaf mesophyll of B. notosergila. They were

reported positive test for lipophilic compounds mentioned for the genus by Budel et al. (2018)

in basal cells. Tosoratto et al. (2016) studying B. and Ornellas et al. (2019). According to Pihakaski

salicifolia described the ﬂagelliform trichomes et al. (1987), there is a seasonal ﬂuctuation in

as glandular bulbiferous ﬂagelliform. Budel et storage lipids, it would be increasing in the growing

al. (2018) described and illustrated the secreted period. It may be seen large lipid bodies in summer

substances in the body and apical cell of the but several small spherules in winter. Lersten et

ﬂagelliform trichomes, and they suggested that al. (2006) referred the presence of oil bodies in

these ﬂagelliform glandular trichomes have two leaf mesophyll cells of many Angiosperms, and

functional properties for protection and secretion. indicated the Asteraceae as one of the families

They also reported two forms of ﬂagelliform in which the highest number of species have

trichomes, type I and type II, with straight and lipid bodies. Gidda et al. (2016) reported that

curved body, respectively. Ornellas et al. (2019) environmental conditions such as dark and extreme

also cited the glandular ﬂagelliform trichomes temperatures (heat and cold) induce oil body

in other species of Baccharis. The lipophilic formation, so they also suggested leaf oil bodies

substances secreted by glandular trichomes function in stress response. The function of the leaf

and deposited on the leaves form an oily layer oil bodies still are under study, however, Shimada et

that increase the impermeability and reduce al. (2014) showed that the leaf oil bodies function

transpiration (Haberlandt, 1928). In this way, as subcellular factories for the production of a

trichomes help prevent leaf overheating and novel stable phytoalexin (antimicrobial compounds

water loss by transpiration process (Johnson, that are synthesized after stresses) in response to

1

975; Ehleringer & Mooney, 1978; Fahn & fungal infection and senescence. Shimada et al.

Cutler, 1992; García et al., 2008). Glandular (2018) reported that oil bodies are lipid storage

trichomes are an important source of essential compartments that occur primarily in seeds and

oils having diﬀerent uses, although many of these senescing leaves, and concluded the oil bodies

substances have evolved to provide the plant with have multiple functions, in seeds, seedlings and in

protection against herbivores and pathogens (Glas leaf. In the leaves, the energy accumulated in oil

et al., 2012). Trichomes may also complement the bodies has a defensive role against fungal infection

chemical defense of a plant by possessing internal because they produce antifungal compounds.

secretion of phenolics, alkaloids and other repellent

substances (Levin, 1973; Delbon et al., 2012).

Secretory ducts and chemical substances

Minteguiaga (2019) studying species of Baccharis secreted. The secretory ducts were found in leaves

found the oil droplets secreted by trichomes are and stems of B. notosergila. They were previously

essential oils that have bioactive properties (e. g., found in the roots of B. notosergila by Carbone et

garrapaticide, insecticide, fungicide) for example al. (2019). In cross sections of leaves, frequently,

in B. dracunculifolia DC., and B. tridentata Vahl.

there is one duct associated to each vascular

437

Bol. Soc. Argent. Bot. 56 (4) 2021

bundle, but may be seen two or three at middle of the genus by Tosoratto et al. (2016), Budel et

vein level and coincidently in the main vascular al. (2018), and Ornellas et al. (2019). Tannins are

bundle of the petiole. The presence of more than phenolic compounds of high molecular weight,

one duct was previously documented by Budel et and may be found in all organs of plants. The

al. (2018) and reported by Ornellas et al. (2019) presence of tannins is an adaptation to the high

for B. platypoda DC. and B. stylosa Gardner. It incidence of sunshine to protect against oxidative

has been established for Asteraceae the principal stress aﬀecting the photosynthesis (Hassanpour

substances secreted are volatile oils (Budel et al., et al., 2011). The sites of tannin production were

2

012; Jasinski et al., 2014). The secretory ducts the large cells located in the leaf mesophyll,

in B. notosergila have given positive reaction for plants can accumulate phenolic compounds in the

resins, polyphenols, and oils. It was also found in leaf epidermis and mesophyll tissues, where its

B. notosergila subterranean system by Carbone et protective feature became evident against the UV

al. (2019), and it is in agreement with Ariza Espinar radiation damage (Hassanpour et al., 2011). Del

(1973) who reported that the secretory ducts may Valle et al. (2020) established the UV radiation

be releasing other chemical components such as increased the concentration of phenolic compounds

tannins and resins besides essential oils. The resins (tannins, ﬂavonoids, anthocianins) suggesting a

could protect the plant against insects as occur in photoprotective role against UV light. On the other

coniferous (Johnson & Croteau, 1987). Cobos et hand, secondary metabolites of phenolic nature

al. (2001) analyzed the composition of the essential play an important role in the defensive response, e.

oils in aerial organs of B. notosergila, and they g., phytoalexins who behave as inducer or elicitors

found 32 constituents and α-pinene, limonene, of plant defense mechanisms (Ebel, 1986; Boller,

β-caryophyllene, and the spathulenol as the major 1989; Stone, 1989). Currently, research suggests

components. Budel et al. (2018) and Minteguiaga that phytoalexins are a biochemical mechanism

(

2019) indicated that Baccharis species produce possessed by plants for disease tolerance and

volatile oils that mainly contain sesquiterpenes pathogen attacks (Ryan, 1987).

and monoterpenes. Internal secretion of terpens

By other way, during the ﬁeldwork was found

and other secondary metabolites (e. g., ﬂavonoids, a reduction of Stipa population around the B.

tannins, resins) would help protect the plant from notosergila plants (M. Oyhamburu & F. Fernández,

herbivores and pathogens, and contributing to the personal communication, October 20, 2020). This

water balance (Fahn & Cutler, 1992; Delbon et is a new line to research, on the basis that numerous

al., 2012; Tosoratto et al., 2016). Essential oils compounds of phenolic nature act as allelopathic

components are produced in most plant organs and agents inhibiting the germination and growth of

they are stored in secretory structures (glandular other species around plants (Rice, 1984). Although

trichomes and internal ducts). Chemically essential there are few reports the Baccharis species

oils are complex mixture which have biology allelopathic eﬀects, Dias et al. (2017) probed an

eﬀects (e.g., antimicrobial, analgesic, antioxidants, allelopathic potential of phenolic compounds using

sedative, antiinﬂamatory, andmutagenic, phototoxic an ethanolic and aqueous extracts from aerial parts

and citotoxic) (Budel & Duarte, 2008; Minteguiaga, of Baccharis spp.

2

019). In Baccharis has been isolated and identiﬁed

more than 500 compounds, the most frequent

would be essential oils, terpenoids, and ﬂavonoids cells of stomata, in the chlorenchyma of leaves and

Starch grains. These were identiﬁed in the guard

(Minteguiaga, 2019).

stems, in the last also in the secondary phloem.

However, this polysaccharide was not detected in

Phenolic compounds. Tannins were identiﬁed subterranean organs (Carbone et al., 2019). We

in the epidermal tissue and mesophyll of leaves. did not ﬁnd starch grains in the parenchyma sheath

In stem in the secondary protection tissues, and surrounding the vascular bundles as was cited by

were also found in the secondary xylem which is in Budel et al. (2018). Thus, we believe the starch

agreement with the localization reported by Carbone grains presence and quantity is variable in relation

et al. (2019) in the xylopodium of B. notosergila. with the period of the year in which the leaves and

Similar results were reported in diﬀerent species aerial stems are collected.

438

A. V. Carbone et al. - Baccharis notosergila: aerial vegetative organs and environment

Calcium oxalate crystals (CaOx). Crystals epidermal cells with straight cell walls; massive

were found in the mesophyll of leaves, in pith and and striate cuticle; glandular trichomes secreting

medullary rays of stems, and in the head cells of oily substances; stomata at level or above the

the glandular capitate trichomes of B. notosergila. other epidermal cells; presence of tannins in

Carbone et al. (2019) recorded abundant styloids leaves and stem tissues; oily bodies in mesophyll

in medullary rays of the xylopodium and roots of cells; a moderate quantity of ﬁbers; presence of

the same species. These crystal types and others endodermis with Casparian strips; amphistomatic

were revealed for the genus by previous authors, leaves and isobilateral mesophyll. Among them

coincidentally in the mesophyll of leaves, and the epidermal tissue, cuticle and epicuticular

the perimedullary region of stems (Cortadi et waxes covered by an oily layer, and presence of

al., 1999; Budel et al., 2003, 2004; Petenatti et tannins would be a physical and chemical barrier

al., 2007; Budel & Duarte, 2010; Jasinski et al., for dehydration as well as the penetration of the

2

014; Bobek et al., 2015, 2016; Budel et al., herbicides applied for its control. The mentioned

015, 2018). Many reasons have been written characteristics adding the abundant lipophilic

about the formation and functions of CaOx in substances, the presence of ﬁbers and endodermis

plants, such as the functions attributed to the in stems would be producing tolerance to lowland

calciﬁcation process include the elimination of areas and the alternate of drought and ﬂooding

oxalate in those plants unable to metabolize it, periods which are common in the studied region.

protection against herbivores (Molano-Flores, The stomata localized at level or slightly elevated

2

001), being a source of calcium reserve (Volk and scarce sclerenchyma are mesomorphic traits

et al., 2002), the detoxiﬁcation of heavy methals corresponding to a luminous temperate weather in

Nakata, 2003). Franceschi & Nakata (2005) which B. notosergila inhabit, and the combination

(

communicated the crystals are formed in speciﬁc amphistomatic leaves with isobilateral mesophyll

shapes and sizes, and genetic regulation of CaOx promote more eﬃcient photosynthesis process. As

formation is indicated by constancy of crystal a matter of fact, leaves are present during spring-

morphology within species. The same authors, summer, with favorable environmental conditions

also mentioned as the major functions of CaOx contributing plants produce as many resources as

crystals in plants include high-capacity calcium possible to storage in its deep root system, ensuring

regulation, and protection against herbivores. the survival during the unfavorable period, and

Apóstolo (2005) reported high pH values in the providing the capacity to sprout and resprout from

soil promote formation of crystals in plants, and the bud-bank (xylopodium), restoring the plant

Garcia et al. (2008) indicated the presence of aerial parts in the following spring.

crystals in leaf mesophyll would be associated to

saline/alkaline soils. In B. notosergila, we have

seen small crystals in mesophyll cells of leaves author contributionS

collected in sweet lowland and half hill, but not

observed in the leaves from alkaline-saline soils.

AVC provided the global research ideas and

On the basis of these data we infer that there might goals, and with FEF provided the resources and

be several factors promoting the formation of ﬁeldwork data and interpretation. MPH, SMMA

calcium oxalate crystals.

and AMA carried out the laboratory research.

AMA, AVC and MPH prepared the ﬁrst manuscript.

All authors have read and contributed to write the

ﬁnal manuscript.

concluSionS

This study allows us to achieve an interpretation

about the adaptive characteristics of B. notosergila acKnowledgementS

whichshowshigherstresstoleranceandcompetitive

ability. A number of meso-xeromorphic characters

We thank the technicians Mario Sánchez and

are found in B. notosergila, such as small, narrow Mariela Theiller of CINDECA-CONICET-UNLP

and deciduous leaves; the hydathodes presence; for the electron microscope service.

439

Bol. Soc. Argent. Bot. 56 (4) 2021

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