Floral nectary Structure, nectar PreSentation and

morPho-anatomical analySiS oF male-Fertile and male-

Sterile antherS in onion (allium cePa, amaryllidaceae)

eStructura del nectario Floral, PreSentación del néctar y

análiSiS morFo-anatómico de anteraS de líneaS androFértileS y

androeStérileS en cebolla (allium cePa, amaryllidaceae)

1

2

3

Ana M. Gonzalez * , Irma B. Maldonado , Claudio R. Galmarini

&

4

Iris E. Peralta

Summary

Background and aims:The onion (Allium cepa var. cepa) is an allogamous species in

which male-sterile lines have been developed. However, the structure of the ﬂower

and ﬂoral nectaries have only been brieﬂy described. The objective of this study is

to update the ﬂoral anatomy data, comparing the gynoecium and androecium of

male-fertile and male-sterile lines, and to analyze the three-dimensional structure

of the ﬂoral nectary.

M&M: Conventional optical and scanning electron microscopy techniques were used.

Results: Fertile and sterile male ﬂowers have the same structural organization. The

septal or gynopleural nectary is organized in three zones: 1) production area formed

by the glandular tissue arranged radially in the septa of the ovary, 2) discharge

zone: a small channel at the apex connects the nectariferous tissue with the pocket

formed between the ovary wall and the overlying ridge, and 3) presentation and

harvest zone, where the excreted nectar accumulates, formed between the widened

base of the inner staminal ﬁlaments opposite the ovary.

1

. Facultad de Ciencias Agrarias,

Universidad Nacional del

Nordeste; IBONE (UNNE-CONICET).

Corrientes, Argentina

2

. Instituto Nacional de Tecnología

Agropecuaria, AER Formosa,

Argentina

3

. Instituto Nacional de Tecnología

Agropecuaria, EEA La Consulta;

Facultad de Ciencias Agrarias,

Universidad Nacional de Cuyo;

CONICET. Mendoza, Argentina

4

. Facultad de Ciencias Agrarias,

Universidad Nacional de Cuyo,

IADIZA (CONICET). Mendoza,

Argentina

Conclusions: The only anatomical diﬀerences in the ﬂowers sterile male lines are

the lack of pollen production and the absence of dehiscence, despite having a

normal stomium and anther wall. The ﬂoral nectaries of onion are a clear example

of secondary presentation of nectar.

*anagonzalez.ibone@gmail.com

Key wordS

Citar este artículo

GONZALEZ, A. M., I. B.

MALDONADO, C. R. GALMARINI &

I. E. PERALTA. 2023. Floral nectary

structure, nectar presentation

and morpho-anatomical analysis

of male-fertile and male-sterile

anthers in onion (Allium cepa,

Amaryllidaceae). Bol. Soc. Argent.

Bot. 58: 477-489.

Anther, dehiscence, gynopleural nectary, nectary pocket, onion, septal nectary.

reSumen

Introducción y objetivos: La cebolla (Allium cepa var. cepa) es una especie alógama,

donde se han desarrollado líneas androestériles. La estructura ﬂoral y la de sus

nectarios ﬂorales ha sido descrita de manera somera e incompleta. El objetivo del

presente trabajo es actualizar los datos de la anatomía ﬂoral comparando líneas

fértiles y androestériles y analizar la estructura tridimensional del nectario ﬂoral.

M&M: Se utilizaron técnicas convencionales de microscopía óptica y electrónica de

barrido.

DOI: https://doi.

org/10.31055/1851.2372.v58.

n3.38251

Resultados: Las ﬂores fértiles y androestériles presentan la misma organización

estructural. El nectario septal o ginopleural se organiza en tres zonas: 1) área

productora formada por el tejido glandular dispuesto radialmente en los septos

del ovario, 2) zona de descarga: un pequeño canal en el ápice conecta el tejido

nectarífero con el bolsillo formado entre la pared del ovario y la cresta que los

cubre, y 3) zona de presentación y cosecha, donde el néctar excretado se acumula,

formada entre la base ensanchada de los ﬁlamentos estaminales internos y la base

del ovario.

Conclusiones: Las únicas diferencias anatómicas en las ﬂores de las líneas

androestériles y las fértiles radican en la falta de producción de granos de polen y

la ausencia de dehiscencia, pese a presentar estomio y pared de anteras normales.

Los nectarios ﬂorales de la cebolla son un claro ejemplo de presentación secundaria

del néctar.

Recibido: 11 Abr 2023

Aceptado: 16 Mar 2023

PalabraS clave

Antera, bolsillo nectarífero, cebolla, dehiscencia, nectario ginopleural, nectario septal.

Publicado en línea: 1 Jun 2023

Publicado impreso: 30 Sep 2023

Editores: Nicolás García Ber guecio

&

Agostina Sassone

ISSN versión impresa 0373-580X

ISSN versión on-line 1851-2372

477

Bol. Soc. Argent. Bot. 58 (3) 2023

introduction

anthers fails, and the pollen production is aborted

Holford et al., 1991).

Offering rewards such as nectar is one of the

(

The onion (Allium cepa L. var. cepa) is one of

the most cultivated horticultural species to produce plant’s resources for attracting pollinators (Fahn, 1979;

bulbs (Galmarini, 2018). According to FAO, world Bernardello, 2007; Pacini & Nepi, 2007; Nepi et al.,

production in 2021 was 151 million tons, covering 2012). There are numerous studies on various species

approximately 6 million ha; in Argentina, 16,000 ha that show that the size, shape or color of diﬀerent

of onions were cultivated in 2021 with a production of ﬂoral parts are related to pollinator visits (López &

600,000 tons (FAOSTAT, 2021). The implantation of Galetto, 2002; Pernal & Currie, 2002; Silva et al., 2003;

the crop can be done by sowing seed or planting bulbs. Abrol, 2005; Poveda et al., 2005; Ford & Johnson,

Argentina not only stands out for the production of 2008; Human & Nicolson, 2008; Steenhuisen et al.,

bulbs but also for seed production, the most important 2010). The ﬂowers of many monocotyledons present

areas are located in central-western provinces of San gynopleural ﬂoral nectaries (GN), also called septal

Juan and Mendoza. Fertile or open-pollinated cultivars nectaries (Van Heel, 1988; Smets et al., 2000). The

and also ﬁrst-generation hybrids (F1), produced by GN are nectar-secreting cavities consisting of the

crossing pure or partially homozygous lines with a incomplete fusion of the carpel walls in the septal

male-sterile line (MSL), are used for seed production. region (Smets & Cresens, 1988; Pacini & Nepi, 2007;

Male sterility was discovered in onion in 1925 (Saini Odintsova et al., 2013; Fishchuk & Odintsova, 2020).

&

Davis, 1969) and since then it has been a valuable Fritsch (1992) compared the position of the GN of

resource for hybrid seed production (Havey, 2000; 160 species of Allium, including A. cepa, highlighting

Kamenetsky & Rabinowitch, 2002; Kik, 2002; the importance of this characteristic in the confusing

Engelke et al., 2002, 2003). Onion hybrid seeds have taxonomy of the genus Allium (Gurushidze et al., 2007).

been extensively produced all over the world using Contrary to the scant recognition of structural studies on

cytoplasmic–genic male sterility (CGMS) based ﬂoral nectaries of onion, there is a profuse bibliography

systems. There are two main sources of cytoplasmic of nectar chemistry and the relationship with pollinators

male-sterility identiﬁed as S and T, which have been (Syamasundar & Panchaksharappa, 1976; Kumar &

genetically characterized. S type results from the Gupta, 1993; Silva et al., 2000, 2004; Soto et al., 2015;

interaction of a cytoplasmic factor S and a single Gillespie et al., 2015, Divija et al., 2022).

nuclear restorer gene Ms (Colombo & Galmarini,

In many cases, the structure of the ﬂowers is

2017, and references therein). The system of CGMS is organized in such a way that the place of nectar

deﬁned as the inability to produce viable pollen grain production is diﬀerent from the place of its presentation,

in plants. The lower average seed yield in F1 hybrids i.e., where the nectar accumulates and is oﬀered to the

may be the result of deﬁcient pollination and factors visitors, which is called secondary presentation (Fahn,

related to ﬂower morphology or nectar composition of 1979; Vogel, 1998; Pacini & Nepi, 2007). Kavitha

the MSL (Parker, 1982; Céspedes et al., 2004; Soto et & Reddy (2018) described Allium ﬂowers as bowl-

al., 2013, 2015; Gatica Hernandez et al., 2019).

shaped with the nectary hidden in the lower part of

Onion flowers are grouped in umbels, which the ovary. The nectar produced accumulates in the

have between 50 and 2,000 flowers (Fig 1A-B; cup located between the base of the ovary and the

Brewster, 2001; Kavitha & Reddy, 2018). Flowers inner whorl of stamens, which have staminal ﬁlaments

are protandric: in the fertile variety the anthers mature with a widened base (Fig. 1B). According to Brewster

normally and pollen is released before the stigma (2001), this area is easily accessible to many types of

becomes receptive (Currah & Ockendon, 1978). pollinating insects. It has been demonstrated that there

The ﬂower bears a perigonium consisting of two is variability between the fertile and male-sterile onion

whorls of three tepals; the androecium is composed lines regarding the preference of bees to visit their

of two whorls of three stamens, and the gynoecium ﬂowers (Soto et al., 2013, 2015, 2021).

is composed of three carpels fused in a superior

The aim of the present study is to extend the

ovary, with axillary placentation and two ovules per morpho-anatomical descriptions of Allium cepa

locule (Gaviola, 2007). In plants that are good seed ﬂowers, to re-evaluate the three-dimensional structure

producers, there are usually three to four mature seeds of the gynopleural nectary in relation to the ﬂoral parts

in each fruit. In male-sterile plants, dehiscence of the and to explain the phenomenon of secondary nectar

478

Ana M. Gonzalez et al. - Floral nectary and anthers anatomy of Allium cepa

Fig. 1. Allium cepa. A: Inﬂorescence of fertile variety. B: Flowers, the red arrow indicates the inner stamen

with a broad base and the blue arrow to the outer stamen with a thin staminal ﬁlament. Scales= A: 0.5 cm,

B: 0.1 cm.

presentation. It is also intended to determine whether series, critical-point dried using liquid CO and sputter

2

there are diﬀerences in the structure of the nectary in coated with gold–palladium. The gold-coated samples

fertile cultivars and male-sterile lines. In addition, the were photographed with a SEM Jeol LV5800 (JEOL

ﬂoral anatomy will be studied in depth with emphasis Ltd., Tokyo, Japan), at 20 Kv in the Service of Electron

on the anthers of the fertile and male-sterile lines to Microscopy facility at Universidad Nacional del

understand the availability of pollen in the varieties Nordeste (Corrientes, Argentina).

cultivated in Argentina.

reSultS

materialS and methodS

Floral morphology and anatomy

Four onion accessions were used, one male-

fertile variety (FV, Valcatorce INTA; Galmarini, male-sterile lines is the same, the diﬀerence lies in the

000) provided by INTA EEA La Consulta and pollen production. The ﬂowers of A. cepa have two

The morphological structure of fertile ﬂowers and

2

three male-sterile lines (MSL, ON.192A, ON.013A, whorls of free tepals, three outer and three inner, white

and ON.108A) provided by the Enza Zaden Seed with a green central line on both sides (Fig. 1B).

Company. Vouchers (ﬁxed material) were deposited at

The androecium consists of two whorls of three

CTES herbarium, voucher number: Valcatorce INTA stamens each, those of the outer whorl have slender

AMG Nº 528, ON.192A AMG Nº 529, ON.013A staminal ﬁlaments. The three inner stamens have

AMG Nº 530, and ON.108AAMG Nº 530.

tricuspidate staminal ﬁlaments, with basally widened

Flowers of A. cepa were fixed in FAA tepaloid expansions ﬁnishing in two free ends and

(formaldehyde, alcohol 70%, acetic acid, 90:5:5). a third that lengthens and supports the anther (Figs.

The material was dehydrated through a tertiary 1B; 2A-C). The widened bases of the inner staminal

butanol series and embedded in paraﬃn (Gonzalez ﬁlaments form a cup-shaped area where the ﬂoral

&

Cristóbal, 1997; Ruzin, 1999), microtomized nectar accumulates. The anthers are bithecal, versatile,

using a Microm HM350 rotary microtome in 12 µm and dorsiﬁxed (Fig. 2A-C). In both FV and MSL

transversal (TS) and longitudinal sections (LS), and ﬂowers, a dehiscence line is visible externally on the

ﬁnally stained in safranin and astra blue combinations anthers, but thecae of the MSL do not open or release

(Luque et al., 1996). A Leica MZ6 light microscope pollen grains (Fig. 2B-C).

(

LM) with a digital imaging system was used for the

Both FV and MSL present the same anatomy

in the anther wall and the stomium zone, the

observations.

For scanning electron microscopy (SEM), FAA- diﬀerences between them are due to the process of

ﬁxed material was dehydrated in an increasing acetone microgametogenesis (Fig. 2D-M).

479

Bol. Soc. Argent. Bot. 58 (3) 2023

In mature anthers of FV, the wall of the thecae is

The complex organization of the nectary can only

only composed of an exothecium and endothecium be understood by analyzing the exomorphology of

Fig. 2 D-F). The exothecium bears cells with thickened the gynoecium and its anatomy through a sequence of

(

cellulosic walls which are covered with a finely transversal and longitudinal serial sections of the ovary

reticulated cuticle, which lacks stomata (Fig. 2G). The (Figs. 3-4).

endothecium is composed of a single layer of thin-

Externally the ovary has three grooves that protrude

walled cells with U-shaped ligniﬁed thickenings; the at the edges, which accompany the dorsal bundle of

bars of these thickenings are free, covering the inner each carpel along its path (Figs. 3A-F, 4J-L). The carpel

tangential wall and the side walls without reaching wall in the dorsal bundle area presents an external

the outer tangential wall (Fig. 2H). The stomium zone groove, which is the only area of the epidermis with

in FV has small epidermal and endothecial cells and stomata that lack a substomatal chamber.

longitudinal dehiscence occurs through these cells (Fig.

The lateral sides of the ovary are ﬂat and are

2F). In the ripe anther of FV, orbicules are observed constitutedbytwoadjacentcarpels, withoutdelimitation

covering the inner walls of the pollen sacs. Pollen of the suture line (Fig. 3B-D). By removing the ovary

is monosulcate and oblate in shape, with a rugulate and observing it from the base, three elongated and

sculpture (Fig. 2I).

pocket-shaped openings are visible; they consist of

The anthers of FV have the same organization crests of carpellary tissue that cover the ovary laterally,

in the anther wall and stomium zone (Fig. 2J-L) delimiting three cavities or nectar pockets (Fig. 3C-E).

Despite having an endothecium with well-developed Each crest corresponds to two contiguous carpels (Fig.

thickenings, there is no dehiscence. The stomium 3C).

also has small-sized cells. The diﬀerence with fertile

In cross-sections of the ovary it is observed that the

anthers lies in the volume of the pollen sacs. The sacs portion of two adjacent carpels folds inwards forming

have collapsed and there is cellular debris inside. In the septum and delimiting the axillary placentation

MSL the anthers do not produce pollen; the remains (Figs. 3D-E; J-L). In the septum, the suture between

of sporogenous cells or aborted microspores can be the walls of the carpels is incomplete and forms three

observed, agglutinated by tapetal cellular residues (Fig. grooves, each corresponding to GN or septal nectaries

2M). In the anthers of MSL, the cells of the stomium (Figs. 3D-E; H-K). In this area, the epidermal cells

zone, endothecium, and epidermis are not aﬀected, they are arranged in a palisade (Fig. 3F-G). The epidermis

have the same cellular conformation as in FV; however, and 1-2 layers of subepidermal parenchyma of the

no dehiscence occurs in these anthers.

carpel are diﬀerentiated into nectar-secreting tissue,

The tepals and tepaloid bases of the staminal characterized by a very dense cytoplasm with a central

filaments (in both FV and MSL) have the same nucleus and no perceptible vacuoles; the walls are

anatomical structure: a compact parenchyma, covered cellulosic and thin (Fig. 3F-G).

by a unistratiﬁed epidermis, without stomata (Fig. 2J).

The rest of the septum, as well as the carpel wall, is

The ﬁliform portion of all the staminal ﬁlaments is thin; formed by a compact fundamental parenchyma. Inside

the colorless and compact parenchyma is covered by the pocket, the crest has an inner longitudinal groove

a unistratiﬁed epidermis of cells arranged in palisade, (Fig. 3E). Each crest over the GN consists of 3-4 layers

without stomata, covered with a ﬁnely striated cuticle of ground parenchyma, covered by a unistratiﬁed

(Fig. 2D, J).

epidermis, without stomata; there are no secretory cells

and they lack vascularization (Fig. 3H-J).

Gynoecium and Nectary

In a radial longitudinal section passing through

There is no diﬀerence in the structural or vascular the septum and nectary, it can be seen how the apical

organization between FV and MSL ﬂowers. The ovary portion of GN is connected to the nectariferous pocket

is superior, tricarpellar, trigonous, and slightly ﬂattened. (Fig. 3H-J). The nectar produced and excreted into

The carpels are organized in an axillary placentation the septum area thus ﬁnds a place to exit into the

with two ovules per locule (Figs. 3C, 4). The style is nectariferous pocket and accumulates between the

single and gynobasic, it is located in an invagination ovary and the tepaloid base of the staminal ﬁlaments.

of the apical portion of the ovary; the stigma is an

inconspicuous knob that completes its elongation after the carpels, in its basal portion (Fig. 3A, D, H, K). The

the dehiscence of the anthers occurs (only in FV). ovules are campylotropous with curved nucellus (Fig.

Each locule bears two ovules, inserted in the axils of

480

Ana M. Gonzalez et al. - Floral nectary and anthers anatomy of Allium cepa

Fig. 2. Flowers of Allium cepa. A-C, J-M: SEM; D-I: LM. A-B: Longitudinal section of fertile variety (FV)

ﬂower. C: Androecium and tepals in male-sterile line (MSL) ﬂowers; asterisks in B-C indicate tricuspidate

tepaloid expansions of staminal ﬁlaments. D-I: FV anther. D: Transversal section of almost dehiscing

anther. E: Detail of anther wall showing endothecial cells with ﬁbrous thickenings and pollen grains. F:

Stomium zone. G: Superﬁcial view of anther epidermis. H: Paradermal section showing endothecium with

ﬁbrous thickenings. I: Pollen and inner face of tapetal membranes. J-M: MSL anther. J: Tepals and anther

with collapsed pollen sacs. K: Detail of anther and collapsed pollen sac. L: Indehiscent stomium zone.

M: Abortive microspores inside MSL anther. Abbreviations: ct: collapsed tissue, et: exothecium, is: inner

stamen, it: inner tepal, np: nectary pocket, nt: endothecium, os: outer stamen, ot: outer tepal, ov: ovule, ova:

ovary, s: stomium, sf: staminal ﬁlament, st: style. Scales= A-C: 500 µm; D, J: 200 µm; E-F, K-L: 50 µm; G-H:

20 µm; I, M: 10 µm.

481

Bol. Soc. Argent. Bot. 58 (3) 2023

Fig. 3. Gynoecium and gynopleural nectary of Allium cepa. A-F, I, K: SEM; G, H, J, L: LM. A: Longitudinal

section of fertile variety (FV) ﬂower; the asterisk shows the aperture for nectar exit. B: Apical view of ovary.

C: Basal view of ovary showing the nectary pocket apertures; white lines indicate the limits between carpels,

white arrowpoint indicate dorsal slots (in B-D). D: Transversal section (TS) of ovary. E-F: False color in SEM

images: pink = cytoplasm, blue = nucleus. E: Detail of the ovary in TS showing the gynopleural nectary (GN:

pink cells) and nectary pocket covered by ﬂat crest. F-G: Glandular epidermis of GN. H: Longitudinal section

of male-sterile line (MSL) ﬂower indicating an ovule in the left lobe and the nectary to the right, covered by a

crest (arrow), the nectar accumulation area between ovary and anther is indicated by an asterisk. I: Nectary

pocket and crest in detail. J: Detail of H showing GN; arrow indicates the apical opening for nectar exit to the

nectary pocket (asterisk). K-L: Ovule. Abbreviations: cr: crest, gn: gynopleural nectary, it: inner integument,

np: nectary pocket, ob: obturator, ot: outer integument, ov: ovule, st: style. Scales= A-D: 500 µm; E, H, J:

200 µm; I, K-L: 100 µm; F-G: 20 µm.

482

Ana M. Gonzalez et al. - Floral nectary and anthers anatomy of Allium cepa

3K-L). Both integuments have between 6-8 layers of

In the longitudinal section of the gynoecium, the

thickness, which are multiplied in the micropyle. The style is inserted in the center of the ovary, almost at

external epidermis of the inner integument presents the base, due to the invagination of the carpellary wall

cells arranged in a short palisade. The nucellus is (Fig. 3A, H). The style is hollow, the central channel

inconspicuous, only one layer of cells separates the is covered with cells whose radial walls are loosely

embryo sac from the endostome. The chalaza has arranged; the entire inner part of this epithelium and the

small cells of dense cytoplasm, with the appearance spaces between the walls are ﬁlled with mucilage. The

of hypostasis; this tissue even reaches the vascular stigma is lined by cells with convex outer walls and,

bundle. The epidermis of the placenta is diﬀerentiated consequently, has a papillose surface.

in secretory tissue, constituting a placental obturator

Fig. 3L).

Floral vascularization (Fig. 4): the ﬂower peduncle

is innervated by 6-9 vascular bundles, which are united

(

Fig. 4. Allium cepa ﬂoral vascularization and gynopleural nectary (GN) position. A: Longitudinal section of ovary

showing diﬀerent levels of transverse sections in diagrams B-L: (glandular tissue shaded, vascular bundle in

black) and transversal sections (M-R). A-D: Peduncle region. E-F: Receptacle. G-J: Ovary and staminal ﬁlaments,

tepals were not drawn. K-L: Ovary. M-R: LM of gynopleural nectary transection; nectary pocket is indicated with

asterisk. Abbreviations: cr: crest, cs: nectar accumulation area, dc: dorsal carpellary vascular bundle, ﬁs: broad

base of inner staminal ﬁlament, fos: thin outer staminal ﬁlament, gn: gynopleural nectary, it: inner tepal, ot: outer

tepal, np: nectary pocket, ov: ovule, ova: ovary, st: style. Scales= A-L: 1 mm; M-R: 0.5 mm.

483

Bol. Soc. Argent. Bot. 58 (3) 2023

forming a hexagonal ring in the receptacle (Fig. 4A-D). which a dehiscence line is recognized externally;

Six traces are detached towards the periphery, each anatomically, this region is the stomium, structurally

one is divided periclinally, the six external traces typical with smaller cells. The endothecium of the

vascularize the tepals and the six internal ones anthers in MSL forms thickenings identical to that

innervate the short staminal tube (Fig. 4E-F). Each of the FV. However, despite this normal anther wall,

stamen remains vascularized by a small bundle dehiscence of the locules does not occur.

that runs through the staminal ﬁlament to the

Anther dehiscence is a process that involves

connective tissue between the anthers. The tepaloid changes in the sterile tissues (endothecium and

projections of the staminal ﬁlaments of the inner development of ligno-cellulosic thickening,

stamens lack vascularization other than that of the septum, and stomium deﬁned as weakened regions

ﬁlaments (Fig. 4G). From the central vascular ring, susceptible to lysis and rupture, general dehydration

three traces separate and become the dorsal bundles of the anther) and sexual cells (mature pollen

of each carpel (Fig. 4F-H). The vascular remnant swelling). This process has been widely studied

adopts a triangular shape dividing into ventral and by several authors (Keijzer, 1987, 1999; Bonner

placental bundles that will innerve the ovules (Fig. & Dickinson, 1989; Scott et al., 2004; Wilson

4

G-L). The style lacks a vascular supply.

In the series of sections in Fig. 4A, M-R, the been put into genetic and molecular studies to

relative positions of the gynopleural nectary and understand the process of cytoplasmic male sterility

et al., 2011). In Allium cepa a great eﬀort has

the nectariferous pocket can be observed.

and its contributions to future breeding programs

Ahmad et al., 2020; Manjunathagowda et al.,

021; Yu & Kim, 2021). However, none of these

(

2

diScuSSion and concluSionS

studies took into account the development of the

exothecium or the cells of the stomium zone. Only

The anatomical study of the flower showed García et al. (2006) studied the mechanism of

that there are no diﬀerences between the male- anther opening, but in Allium triquetrum L., and

fertile and male-sterile lines involving the ﬂoral they associated it with the variation in moisture

structure in general or the gynoecium or nectary content and consequent dehydration, considering

structure in particular. The fundamental diﬀerence that dehiscence is a phenomenon temporarily

between FV and MSL lines is the interruption of independent of the opening of the stomium. Our

male gametogenesis and the process of anther study, which included fertile and male-sterile lines,

dehiscence. The timing of abortion is concentrated shows that, as both types of ﬂowers have the same

in the late stages of microsporogenesis when the anther wall and stomium structures, it is the swelling

callose dissolves and microspores are released into of pollen in the later stages of maturation and the

the anther locules. In the present study, the presence pressure exerted on the thecal walls that contribute

of collapsed microspores was observed among to the dehiscence of fertile anthers. The absence of

cellular remains presumably of tapetal origin. This mature pollen in the MSL prevents dehiscence of

is consistent with previous embryological and the anthers, despite having a structurally normal

anatomical studies in which it was observed that, stomium and endothecium. This anther opening

although meiosis occurred normally, male sterility mechanism is the same as that described for rice by

is produced by hypertrophy of the tapetal cells Matsui et al. (1999).

and/or pollen degeneration (in onion: Monosmith,

Studies carried out on ﬂoral exomorphology that

928; Saini & Davis, 1969; Tchórzewska et al., inﬂuence seed production of hybrid onions, showed

017; in garlic: Shemesh-Mayer et al., 2015; in that there was a high and consistent correlation

1

2

chives: Engelke et al., 2002). The wall structure of among some ﬂoral morphometric characters, bee

fertile and sterile anthers was not analyzed in the visits and seed production; the most interesting

aforementioned studies. In onion, the programmed being the surface of the external anther and the

cell death of the sexual cells does not aﬀect the length of the style (Soto et al., 2018). The length of

development of the anther wall, septum and stomium the style is the morphometric character that allows

zone, which present a normal structure. With respect diﬀerentiation among open-pollinated and male-

to anther dehiscence, the MSLs show anthers in sterile plants, as well as between diﬀerent MSLs in

484

Ana M. Gonzalez et al. - Floral nectary and anthers anatomy of Allium cepa

their ability to attract bees. The length of the inner of the gynoecium. Allium ﬁstulosum does not

tepals presented a negative and highly signiﬁcant develop a crest and pocket like A. cepa.

correlation with the length of the style; the former

Fritsch (1992) analyzed the shape, position, and

ﬂoral character is easier to measure than the length excretory canals of GN in 160 species of Allium,

of the style and could facilitate the selection of highlighting the importance of this character in

lines with greater potential for seed production taxonomic research. This author mentioned that

(

Maldonado, 2014; Soto et al., 2018).

in sect. Cepa (in which A. cepa is included) “the

canal consists of an inner, tube-like part, which

opens from the radial outer side into a pocket-like,

Gynopleural nectaries

Unfortunately, nectaries have not received much tangentially widened outer part ending in the lower

attention in studies of onions. Jones & Emsweller third of the ovary”, this being a unique feature in

(

1936) studied the ontogenetic development of the genus Allium. Unfortunately, he showed this in

ﬂowers, focusing on the macrogametophyte, but a diagram of the longitudinal section of the ovary,

they did not pay attention to the nectaries, despite in which it is diﬃcult to understand the actual

their excellent drawings showing the ovary and the three-dimensional structure of this description.

position of the ovules in three dimensions.

The same type of descriptions and drawings can

Septal nectaries, correctly called gynopleurals be found in Di Fulvio (1973). Recently, Fishchuk

(

Smets & Cresens, 1988), are present in most (2022) published the vascularization of the ﬂowers

monocotyledon orders (except Liliales) and of A. cepa and established three vertical zones in

thus in many families, such as Amaryllidaceae, the gynoecium: 1) a synascidiate zone at the locule

Asparagaceae, Asphodelaceae, and Iridaceae, base, 2) a symplicate structural zone, which contains

among others (Weberling, 1992; Vogel, 1998; the ovules, and 3) a hemisymplicate zone, which

Smets et al., 2000; Rudall, 2002; Bernardello, 2007; occupies the upper part of the locule; our results

Odintsova et al., 2013: Fishchuk & Odintsova, agree with these observations in both FV and MSL.

2

020, 2021).

In the genus Allium, there is variation in the the production, secretion, and presentation of nectar

form of the gynoecium and also in the presence are organized in three well-deﬁned regions:

or lack of appendages or ovarian processes Nectar-producing zone: located in the three

Fritsch, 2001; Choi et al., 2011, 2012). These interlocular septa, radially arranged and separating

The onion ﬂower has a complex organization and

(

processes may be either absent (naked ovary) or the locules of the ovary. The glandular tissue

present, in which case they can be of two types: is composed of the epidermis and subdermal

apical crest-like (characteristic of northern North parenchyma, in the area formed by the incomplete

American species) or basal hood-like processes suture line between carpels. This area is the site of

(

in northeastern Asian species, subgenus Cepa, nectar secretion and the septal (GN) nectary itself.

in which A. cepa is included). Choi et al. (2011, The nectar outlet is in the apical zone and is hidden

012) stated that the septal nectary opening and by the ﬂat crest.

development of ovarian processes have taxonomic Nectar-discharge zone: constituted by the three

2

importance; however, despite the importance of nectary pockets, covered by a ﬂat crest consisting

this feature it has not received attention in other of the walls of adjacent carpels that cover the lateral

structural and anatomical studies.

walls of the ovary. The interior of this pocket - both

In particular, in A. cepa the structure of GN was the ridge tissue and the walls of the ovary - lack

ﬁrst analyzed by Syamasundar & Panchaksharappa nectar-secreting tissue. Each pocket connects to the

(

1976). Based on nectary histochemistry, these production area in a short section located at the top

authors only mentioned the existence of three septa of the secretory area. This second zone opens to the

with nectariferous tissue. Heel (1988) analyzed the outside at the base of the ovary, through three large

ontogeny of the pistil in several monocotyledons openings or pockets.

with septal nectaries, including Allium ﬁstulosum

Accumulation and harvest zone: nectar produced

L. In this species, the GN opening is narrow and in the GN and expelled through the apical opening

only covered by a small ovarian process (called an passes through pockets and accumulates in a third

epidermal ﬂap), which formed late in the ontogeny collecting zone. These areas are composed by the

485

Bol. Soc. Argent. Bot. 58 (3) 2023

widened base of the three inner stamens, opposed manuscript. IM, CG & IP: collected ﬁeld material

to the aperture of the nectaries. In this area, the and reviewed the text.

excreted nectar can be collected by insects that visit

the ﬂower.

The vertical zoning of the GN was described in Primary data availability

the ﬂowers of Dracaena fragrans (L.) Ker Gawl.,

Sansevieria parva N.E. Br. and S. trifasciata Prain

The primary research data are available in

(Asparagaceae) by Odintsova et al. (2013). These CONICET's institutional repository: https://

authors also recognize three zones: 1) the distinct ri.conicet.gov.ar/handle/11336/193050.

nectary formed by three cavities at the base of the

ovary, 2) the zone of common nectary in the ovary

center where the cavities join, and 3) the external bibliograPhy

nectary zone, that corresponds to the upper part of

the ovary where the septal grooves fuse with the ABROL, D. 2005. Pollination Energetics. J. Asia Pac.

nectariferous cavities and nectary splits opened to

Entomol. 8: 3-14.

the exterior. Unlike A. cepa, in these species there is

https://doi.org/10.1016/S1226-8615(08)60066-7

no accumulation area and harvest zone, since the GN AHMAD, R., M. U. HASSAN, G. B. AKHTAR, S.,

of Dracaena and Sansevieria species lack crests and

pockets. Onion ﬂoral nectaries are a clear example

of secondary presentation of nectar, it is produced

in one place (in the ovarian septa) and oﬀered in

a diﬀerent place (cavities between broad staminal

ﬁlaments and the ovary). In the onion, there is also

SAEED, S. A. KHAN, M. K. N. SHAH & N.

KHAN. 2020. Identiﬁcation and characterization of

important sterile and maintainer lines from various

genotypes for advanced breeding programmes of

onion (Allium cepa). Plant Breed. 139: 988-995.

https://doi.org/10.1111/pbr.12844

another area dedicated to the transport between BERNARDELLO, G. 2007. A systematic survey of ﬂoral

the place of production and the accumulation and

harvesting area. A point that would be interesting for

further research, by means of an ontogenetic study,

is the origin of the crests that cover the nectary

nectaries. In: NICOLSON, S. W., M. NEPI & E.

PACINI (eds.), Nectaries and nectar, pp. 19-128.

Springer, Dordrecht.

https://doi.org/10.1007/978-1-4020-5937-7_2

pockets. The correlation found in some ﬂoral and BONNER, L. & H. DICKINSON. 1989. Anther

chemical traits with onion seed yield reported in

other studies may be a great contribution for onion

breeders, who could select lines that have promising

traits for pollinator attraction and, consequently,

seed yields. Further studies are also required

concerning the heritability of ﬂoral traits.

dehiscence in Lycopersicon esculentum Mill. New

Phytol. 113: 97-115.

https://doi.org/10.1111/j.1469-8137.1989.tb02399.x

BREWSTER, J. L. 2001. Las cebollas y otros alliums.

Editorial Acribia, Zaragoza.

CESPEDES, M., I. PERALTA & C. R. GALMARINI.

2

004. Relación entre la morfología de la flor

acKnowledgmentS

de cebolla y la frecuencia de visitas de abejas

polinizadoras. Horticultura Argentina 23: 65.

To INTA EEA La Consulta (Mendoza, Argentina) CHOI, H. J., A. R. DAVIS & J. H. COTA-SÁNCHEZ.

and Enza Zaden Seed Company for supplying us

with the botanical material. This research was partly

supported by the Universidad Nacional del Nordeste

to AMG (Grants Nº 16A003 and 20P001, SGCyT-

UNNE).

2011. Comparative ﬂoral structure of four new

world Allium (Amaryllidaceae) species. Syst. Bot.

36: 870-882.

https://doi.org/10.1600/036364411X604895

CHOI, H. J., L. M. GIUSSANI, C. G. JANG, B. U.

OH & J. H. COTA-SÁNCHEZ. 2012. Systematics

of disjunct northeastern Asian and northern North

American Allium (Amaryllidaceae). Botany 90: 491-

author contributionS

5

08. https://doi.org/10.1139/b2012-031

AMG: performed the slides, interpreted the COLOMBO, N. & C. R. GALMARINI. 2017. The use

anatomic analysis, made up the ﬁgures and wrote the

of genetic, manual and chemical methods to control

486

Ana M. Gonzalez et al. - Floral nectary and anthers anatomy of Allium cepa

pollination in vegetable hybrid seed production: a

review. Plant Breed. 136: 87-299.

https://doi.org/10.1111/pbr.12473

KNUPFFER (eds.), The genus Allium-taxonomic

problems and genetic resources, pp. 77-85. Proceedings

of an International Symposium, Held at Gatersleben,

Germany, June 11-13. 1991. Institut für Pﬂanzengenetik

und Kulturpﬂanzenforschung, Gatersleben.

CURRAH, L. & D. J. OCKENDON. 1978. Protandry and

the sequence of lower opening in the onion (Allium

cepa L.). New Phytol. 81: 419-428.

https://doi.org/10.1111/j.1469-8137.1978.tb02647.x

DI FULVIO, T. E. 1973. Sobre el gineceo de Allium y

Nothoscordum. Kurtziana 7: 241-253.

DIVIJA, S. D. & P. D. KAMALA JAYANTHI. 2022.

Pollination eﬃciency and foraging behaviour of

honey bees and ﬂies to onion Allium cepa L. J.

Apicult. Res. 61: 688-694.

https://doi.org/10.1080/00218839.2022.2096305

ENGELKE, T., S. HÜLSMANN & T. TATLIOGLU.

FRITSCH, R. M. 2001. Taxonomy of the genus Allium:

contribution from IPK Gatersleben. Herbertia 56:

19-50.

GALMARINI, C. R. 2000. Onion cultivars released by

La Consulta Experiment Station, INTA, Argentina.

HortScience 35: 1360-1362.

GALMARINI, C. R. 2018. Economic and academic

importance. In: SHIGYO, M., A. KHAR & M.

ABDELRAHMAN (eds.), The Allium Genomes.

Compendium of Plant Genomes, pp.1-9. Springer,

Cham. https://doi.org/10.1007/978-3-319-95825-5_1

GARCÍA, C. C., M. NEPI & E. PACINI. 2006. Structural

aspects and ecophysiology of anther opening in Allium

triquetrum. Ann. Bot. 97: 521-527.

2

002. A comparative study of microsporogenesis

and anther wall development in diﬀerent types of

genic and cytoplasmic male sterilities in chives.

Plant Breed. 121: 254-258.

https://doi.org/10.1046/j.1439-0523.2002.00704.x

ENGELKE, T., D. TEREFE & T. TATLIOGLU. 2003.

A PCR-based marker system monitoring CMS-(S),

CMS-(T) and (N)-cytoplasm in the onion (Allium

cepa L.). Theor. Appl. Genet. 107: 162-167.

https://doi.org/10.1007/s00122-003-1230-3

FAHN, A. 1979. Secretory tissues in plants. Academic

Press, London.

FAOSTAT. Food andAgriculture Organization of the United

Nations [on line]. Available from: http://www.fao.org/

faostat. [Accessed: December 2022].

FISHCHUK, O. 2022. Comparative ﬂower morphology in

Allium cepa L. (Amaryllidaceae J.St.-Hil.). Notes in

Current Biology 1: 36-41.

https://doi.org/10.1093/aob/mcl015

GATICA HERNÁNDEZ, I., F. PALOTTINI, I. MACRI, C.

R. GALMARINI & W. M. FARINA. 2019. Appetitive

behavior of the honey bee Apis mellifera in response to

phenolic compounds naturally found in nectars. J. Exp.

Biol. 222: jeb189910.

https://doi.org/10.1242/jeb.189910

GAVIOLA, J. 2007. Ficha técnica, producción de semilla

de cebolla (Allium cepa L.). INTA-EEA La Consulta,

1-18.

GILLESPIE, S., R. LONG & N. WILLIAMS. 2015.

Indirect eﬀects of ﬁeld management on pollination

service and seed set in hybrid onion seed production. J.

Econ. Entomol. 108: 2511-2517.

https://doi.org/10.29038/2617-4723-2022-1-1-6

FISHCHUK, O. S. & A. V. ODINTSOVA, 2020.

Micromorphology and anatomy of the flowers

of Galanthus nivalis and Leucojum vernum

https://doi.org/10.1093/jee/tov225

GONZALEZ,A. M. & C. L. CRISTOBAL. 1997.Anatomía

y ontogenia de semillas de Helicteres lhotzkyana

(Sterculiaceae). Bonplandia 9: 287-294. https://doi.

org/10.30972/bon.93-41497

GURUSHIDZE, M., S. MASHAYEKHI, F. R. BLATTNER,

N. FRIESEN & R. M. FRITSCH. 2007. Phylogenetic

relationships of wild and cultivated species of Allium

section Cepa inferred by nuclear rDNA ITS sequence

analysis. Plant Systemat. Evol. 269: 259-269.

https://doi.org/10.1007/s00606-007-0596-0

(

Amaryllidaceae). Regul. Mech. Biosyst. 11: 463-468.

https://doi.org/10.15421/022071

FISHCHUK, O. A. ODINTSOVA, 2021.

&

Micromorphology and anatomy of the ﬂowers in

Clivia spp. and Scadoxus multiﬂorus (Haemantheae,

Amaryllidaceae). Acta Agrobotanica 74: 7417. https://

doi.org/10.5586/aa.7417

FORD, C. & S. JOHNSON. 2008. Floral traits, pollinators

and breeding systems in Syncolostemon (Lamiaceae).

Plant Syst. Evol. 275: 257-264.

HAVEY, M. J. 2000. Diversity among male-sterility-

inducing and male-fertile cytoplasms of onion. Theor.

Appl. Genet. 101:778-782.

https://doi.org/10.1007/s00606-008-0016-0

https://doi.org/10.1007/s001220051543

FRITSCH, R. M. 1992. Septal nectaries in the genus

Allium. In: HANELT, P., K. HAMMER & H.

HEEL, W. A. VAN. 1988. On the development of some

gynoecia with septal nectaries. Blumea 33: 477-504.

487

Bol. Soc. Argent. Bot. 58 (3) 2023

HOLFORD, P., J. CROFT & H. J. NEWBURY. 1991.

Structural studies of microsporogenesis in fertile and

male-sterile onions (Allium cepa L.) containing the

cms-S cytoplasm. Theor. Appl. Genet. 82: 745. https://

doi.org/10.1007/BF00227320

HUMAN, H. & S. NICOLSON. 2008. Flower structure

and nectar availability in Aloe greatheadii var.

davyana: an evaluation of a winter nectar source for

honeybees. Int. J. Plant Sci. 169: 263-269.

Bras. 10: 199-212.

https://doi.org/10.1590/S0102-33061996000200001

MALDONADO, I. B. 2014. Inﬂuencia de caracteres

ﬂorales y factores ambientales sobre la atracción

de las abejas y la producción de semilla híbrida de

cebolla. Tesis Magister. Universidad Nacional de

Cuyo, Argentina.

https://orcid.org/0000-0001-6830-2927

MANJUNATHAGOWDA, D. C., P. MUTHUKUMAR,

J. GOPAL, M. PRAKASH, ... & M. ANJANAPPA.

2021. Male sterility in onion (Allium cepa L.): origin,

evolutionary status, and their prospectus. Genet.

Resour. Crop. Evol. 68: 421-439.

https://doi.org/10.1086/524113

JONES, H. A. & S. L. EMSWELLER. 1936. Development

of the ﬂower and macrogametophyte of Allium cepa.

Hilgardia 10: 415-428.

https://doi.org/10.3733/hilg.v10n11p415

https://doi.org/10.1007/s10722-020-01077-1

MATSUI, T., K. OMASA& T. HORIE. 1999. Mechanism

of anther dehiscence in rice (Oryza sativa L.). Ann.

Bot. 84: 501-506.

KAMENETSKY, R. & H. D. RABINOWITCH. 2002.

Florogenesis. In: RABINOWITCH, H. D. & L.

CURRAH (eds.), Allium crop sciences: recent

advances, pp 31-57. CABI, Wallingford.

https://doi.org/10.1006/anbo.1999.0943

https://doi.org/10.1079/9780851995106.0031

KAVITHA, S. J. & P. R. REDDY. 2018. Floral biology

and pollination ecology of onion (Allium cepa L.). J.

Pharmacogn. Phytochem. 7: 2081-2084.

KEIJZER, C. 1987. The processes of anther dehiscence

and pollen dispersal. I. The opening mechanism of

longitudinally dehiscing anthers. New Phytol. 105:

MONOSMITH, H. R. 1928. Male sterility in Allium

cepa. Ph.D. Thesis. University of California. United

States.

NEPI, M., P. VON ADERKAS & E. PACINI. 2012.

Sugary exudates in plant pollination. In: BALUŠKA,

F. & J. VIVANCO (eds.), Secretions and Exudates in

Biological Systems, pp. 155-186. Springer-Verlag,

Berlin Heidelberg.

487-489.

https://doi.org/10.1111/j.1469-8137.1987.tb00886.x

KEIJZER, C. J. 1999. Mechanisms of Angiosperm anther

dehiscence, a historical review. In: CLEMENT, C., E.

PACINI & J. C. AUDRAN (eds.), Anther and pollen:

from biology to biotechnology, pp. 55-68. Springer-

Verlag, Berlin Heidelberg.

https://doi.org/10.1007/978-3-642-23047-9_8

ODINTSOVA, A., O. FISHCHUK & A. SULBORSKA.

2013. The gynoecium structure in Dracaena fragrans

(L.) Ker Gawl., Sansevieria parva N.E. Brown and

S. trifasciata Prain (Asparagaceae) with special

emphasis on the structure of the septal nectary. Acta

Agrobotanica 66: 55-64.

https://doi.org/10.1007/978-3-642-59985-9_6

KIK, C. 2002. Exploitationofwildrelativesforthebreeding

of cultivated Allium species. In: RABINOWITCH,

H. D. & L. CURRAH (eds.), Allium crop sciences:

recent advances, pp. 81-100. CABI, Wallingford.

https://doi.org/10.1079/9780851995106.0081

https://doi.org/10.5586/aa.2013.051

PACINI, E., M. NEPI & J. L. VESPRINI. 2003. Nectar

biodiversity: a short review. Plant Syst. Evol. 238:

7-21. https://doi.org/10.1007/s00606-002-0277-y

PACINI, E. & M. NEPI. 2007. Nectar production and

presentation. In: NICOLSON, S. W., M. NEPI & E.

PACINI (eds.), Nectaries and nectar, pp. 167-214.

Springer, Dordrecht.

KUMAR, J. & J. K. GUPTA. 1993. Nectar sugar production

and honeybee foraging activity in 3 species of onion

(Allium species). Apidologie 24: 391-396. https://doi.

org/10.1051/apido:19930405

LÓPEZ, H. & L. GALETTO. 2002. Flower structure

and reproductive biology of Bougainvillea stipitata

https://doi.org/10.1007/978-1-4020-5937-7_4

PARKER, F. D. 1982. Eﬃciency of bees in pollinating

onion ﬂowers. Kans. Entomol. Soc. 55: 171-176.

PERNAL, S. & R. CURRIE. 2002. Discrimination and

preferences for pollen bassed cues by foraging

honeybees, Apis mellifera L. Anim. Behav. 63: 369-

390. https://doi.org/10.1006/anbe.2001.1904

POVEDA, K., I. STEFFAN-DEWENTERA, S. SCHEUB

&T.TSCHARNTKE. 2005. Floraltraitexpressionand

(Nyctaginaceae). Plant Biol. 4: 508-514.

https://doi.org/10.1055/s-2002-34134

LUQUE, R., H. C. SOUSA & J. E. KRAUS. 1996.

MétodosdecoloraçãodeRoeser(1972)-modiﬁcado-

e Kropp (1972) visando a substituição do azul de

astra por azul de alcião 8 GS ou 8 GX. Acta Bot.

488

Ana M. Gonzalez et al. - Floral nectary and anthers anatomy of Allium cepa

plant ﬁtness in response to below- and aboveground

Crop Sci. 61: 3529-3537.

plant-animal interactions. Perspect. Plant Ecol. Evol.

Syst. 7: 77-83.

https://doi.org/10.1016/j.ppees.2005.02.002

RUDALL, P. J. 2002. Homologies of inferior ovaries and

septal nectaries in monocotyledons. Int. J. Plant Sci.

https://doi.org/10.1002/csc2.20597

SOTO, V. C., I. B. MALDONADO, R. A. GIL, I. E.

PERALTA, M. F. SILVA & C. R. GALMARINI.

2013. Nectar and ﬂower traits of diﬀerent onion male

sterile lines related to pollination eﬃciency and seed

yield of F1 hybrids. J. Econ. Entomol. 106: 1386-

1394. https://doi.org/10.1603/EC13096

SOTO, V. C., I. B. MALDONADO, V. P. JOFRÉ, C. R.

GALMARINI & M. F. SILVA. 2015. Direct analysis of

nectar and ﬂoral volatile organic compounds in hybrid

onions by HS-SPME/GC-MS: Relationship with

pollination and seed production. Microchem. J. 122:

110-118. https://doi.org/10.1016/j.microc.2015.04.017

STEENHUISEN, S., R. R. AGUSO, A. JÜRGENS & S.

JOHNSON. 2010. Variation in scent emission among

ﬂoral parts and inﬂorescence developmental stages in

beetle-pollinated Protea species (Proteaceae). S. Afr.

J. Bot. 76: 779-787.

163: 261-276. https://doi.org/10.1086/338323

RUZIN, S. E. 1999. Plant microtechnique and microscopy.

Oxford University Press, Oxford.

SAINI, S. S. & G. N. DAVIS. 1969. Male sterility in

Allium cepa and some species hybrids. Econ. Bot.

23:37-49. https://doi.org/10.1007/BF02862970

SCOTT, R. J., M. SPIELMAN & H. G. DICKINSON.

2004. Stamen structure and function. The Plant Cell

16: S46-S60. https://doi.org/10.1105/tpc.017012

SHEMESH-MAYER, E., T. BEN-MICHAEL, N.

ROTEM, H. D. RABINOWITCH, A. DORON-

FAIGENBOIM, … & R. KAMENETSKY. 2015.

Garlic (Allium sativum L.) fertility: transcriptome and

proteome analyses provide insight into ﬂower and

pollen development. Front. Plant Sci. 6: 271. https://

doi.org/10.3389/fpls.2015.00271

https://doi.org/10.1016/j.sajb.2010.08.008

SYAMASUNDAR, J. & M. G. PANCHAKSHARAPPA.

1976. A histochemical study of floral nectaries

in Dipcadi montanum Dalz. and Allium cepa L.

Cytologia 41: 453-457.

SILVA, E. M. & B. DEAN. 2000. Effect of nectar

composition and nectar concentration on honey bee

(Hymenoptera: Apidae) visitation to hybrid onion

https://doi.org/10.1508/cytologia.41.453

ﬂowers. J. Econ. Entomol. 93: 1216-1221.

https://doi.org/10.1603/0022-0493-93.4.1216

SILVA, E., B. DEAN & L. HILLER. 2003. Honey bee

TCHÓRZEWSKA, D., K. L. DERYŁO & K.

WINIARCZYK. 2017. Cytological and biophysical

comparative analysis of cell structures at the

microsporogenesis stage in sterile and fertile Allium

species. Planta 245: 137-150.

https://doi.org/10.1007/s00425-016-2597-0

VAN HEEL, W. A. 1988. On the development of some

gynoecia with septal nectaries. Blumea 33: 477-504.

VOGEL, S. 1998. Remarkable nectaries: structure,

ecology, organophyletic perspectives III. Nectarioles.

Flora 193: 113-131.

(

Hymenoptera: Apidae) foraging in response to

preconditioning with onion ﬂower scent compounds.

J. Econ. Entomol. 96: 1510-1513.

https://doi.org/10.1093/jee/96.5.1510

SILVA, E. M., B. B. DEAN & L. HILLER. 2004. Patterns

of ﬂoral nectar production of onion (Allium cepa L.)

and the eﬀects of environmental conditions. J. Am.

Soc. Hortic. 129: 299-302.

https://doi.org/10.21273/JASHS.129.3.0299

SMETS, E. F. & E. M. CRESENS. 1988. Types of ﬂoral

nectaries and the concepts ‘character’ and ‘character-

state’- A reconsideration. Acta Bot. Neerl. 37: 121-

https://doi.org/10.1016/S0367-2530(17)30812-5

WEBERLING, F. 1992. Morphology of flowers and

inflorescences. Cambridge University Press,

Cambridge.

1

28.

WILSON, Z.A., J. SONG, B. TAYLOR & C. YANG. 2011.

The ﬁnal split: the regulation of anther dehiscence. J.

Exp. Bot. 62: 1633-1649.

https://doi.org/10.1111/j.1438-8677.1988.tb01586.x

SMETS, E. F., L. P. RONSE DECRAENE, P. CARIS & P. J.

RUDALL. 2000. Floral nectaries in Monocotyledons:

distribution and evolution. In: WILSON, K. L. & D.

A. MORRISON (eds.), Monocots: Systematics and

Evolution, pp. 230-239. CSIRO, Melbourne.

https://doi.org/10.1093/jxb/err014

YU, N. & S. KIM. 2021. Identification of Ms2, a

novel locus controlling male-fertility restoration of

cytoplasmic male-sterility in onion (Allium cepa L.),

and development of tightly linked molecular markers.

Euphytica 217: 191.

SOTO, V. C., I. J. G. GATICA & C. R. GALMARINI.

2021. Onion (Allium cepa L.) hybrid seed production:

Sugar content variation during the ﬂowering period.

https://doi.org/10.1007/s10681-021-02927-4

489