Can flower forms be indicators of pollen diversity and possible gametophytic selection in marigold breeding programs?

doi:10.21203/rs.3.rs-5150631/v1

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Can flower forms be indicators of pollen diversity and possible gametophytic selection in marigold breeding programs?

https://doi.org/10.21203/rs.3.rs-5150631/v1

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Pollen shape has been utilized as a taxonomic attribute since it is thought to be the most constant trait within a plant species. The African marigold (Tagetes erecta L.) has substantial variability within the species due to its wider adaptability to various agroclimatic conditions; thus, from a palynological perspective, this species is interesting for studying the variation in its pollen grains. As a commercial flower crop, the breeding programme involves multiple flower forms within the species; hence, the objective of this study was twofold: first, to characterize the typical pollen grain features of marigold and second, to assess the potential variation in pollen morphology in different flower forms across marigold genotypes for possible gametophytic selection in breeding programmes. Nine African marigold plant genotypes with six different flower forms were imaged using a scanned electron microscope to study the characteristic features of the pollen grains. The pollen grains of Tagetes erecta were found to be radially symmetrical, isopolar monads that were oblate spheroidal and suboblate in shape with tricolpi apertures and with echinate erections on the pollen wall. Significant differences were recorded between the genotypes and flower forms for all the pollen morphological features studied. The variability observed among the pollen grain populations within the genotypes for certain morphometric traits also suggested the potential of using gametophytic selection in marigold breeding programs. Although it is important to establish pollen traits for commercial hybridization programs, little information is available, and to our knowledge, this is the first report on characteristic pollen grain features in African marigolds.

Asteraceae

Intraspecific variability

Marigold

Male gametophyte

Palynology

Pollen grains

African marigold (Tagetes erecta L.), indigenous to Mexico and Guatemala, is one of the most widely distributed members of the Asteraceae family and is cultivated globally. It is an often-cross-pollinated crop that is recognized as one of the most important traditional flowers in Asian countries and as a bright ornamental flower crop worldwide. The inflorescence of marigold plants is the capitulum, which is a flower head composed of numerous flowers, with inner rows of hermaphrodite disc florets and outer rows of male sterile ray florets. Ray florets in general are considered petals that determine the aesthetic value of a flower for its commercial utility. Earlier reports suggested the existence of modified flower forms in marigold viz. single, semidouble, and double types of fertile lines as well as apetaloid and petaloid (modified petals) types of male sterile lines have eased the production of hybrid seeds in marigold, as the sterile forms eradicate the tedious process of emasculation [1, 2]. The development of a hybrid and the success of the hybridization programme are determined by flowering, cross-fertilization, and detailed knowledge about the parents. Although maternal parents have a pronounced effect on the significance of offspring [3, 4], paternal parents can also affect several plant traits, making pollen parents a major contributor to the resulting progeny [5, 6], necessitating the study of pollen grains.

Pollen or microspores are microscopic abundant flower elements that offer an opportunity for male gametophytic selection. These male gametophytes also contain genetic information, which is crucial for sexual reproduction in seed-propagating plants [7]. In the field of palynology, the study of pollen grain characteristics (wall morphology, polarity, symmetry, shape and size) is useful because it provides information on the genetic distinctiveness and ancestry of plant genotypes, which is crucial for the exploitation of germplasm [8], and may be useful in the identification of species because the biological makeup of pollen is intricate and speciesspecific [9]. Variability exists in the pollen grains of different species [10, 11, 12]. In contrast, studies have reported that pollen characteristics, especially the size of pollen grains, vary between genotypes/cultivars within species [13, 14].

The plant life cycle includes a haploid gametophytic phase, during which pollen grains compete for fertilization. This competition, known as gametophytic selection, is hypothesized to be a major driver of plant evolution and genetic variation. The resulting variation in fertilization success due to pollen competition creates the potential for strong directional selection [15, 16]. Earlier studies have reported variations in pollen size, content and vigor within a genotype that are being utilized for gametophytic selection in a breeding program [17, 18, 19, 20]. Pollen grains are highly important for determining the taxonomy of flowering plants and have been used in determining the relationships between genera and species in the Asteraceae family [21]. However, there is no information related to morphometric studies of pollen grains either within or between African marigold genotypes. Considering the multiple flower forms that exist and are essential components in hybrid development in marigolds, it will be interesting to study the structure of pollen grains in relation to their flower forms and utility in crop improvement. Thus, the present study was carried out to determine the basic pollen morphology of marigold plants and to describe the variability in the pollen population within and between genotypes across flower forms.

Marigold plants with different flower forms were collected from the ongoing marigold breeding program at the ICAR-India Institute of Horticultural Research, Bengaluru (13.14°N latitude and 77.50°E longitude), which is located at an elevation of approximately 890 m above mean sea level. The plant material selected for the study comprised nine genotypes representing different flower forms (Table 1). Six genotypes were found to be fertile and maintained by selfing, and the remaining three genotypes were sterile; they were segregated into sterile: fertile (1:1) plants and maintained by intercrossing between them. Fertile flowers were used for the extraction and estimation of pollen grains. Ten random flower buds from each plant were bagged using butter paper to prevent pollen contamination, and fully bloomed flowers were collected at the forenoon when the pollen sacs dehisced. The flowers were held upside down, tapped gently to collect the pollen grains and placed in the desiccator for an hour. The pollen grain samples representing each genotype were dusted on two-sided copper tape and fastened on an aluminum metal plate, and the images were captured with a scanning electron microscope at 5 kV (Hitachi S3000N, Japan). The morphometric parameters of 30 pollen grains from each genotype were measured using Fiji and ImageJ software [22]. The shape of the pollen grains was determined by the equation FI = (P/E) ×100, where FI is the form index, P is the length of the polar axis (the line connecting the proximal and distal pole) and E is the length of the equatorial axis (the line perpendicular to the polar axis) [23]. Depending on the FI values derived, the pollens were classified as oblate-spheroidal (0.89–0.99), spheroidal (1.00), prolate-spheroidal (1.01–1.14), subprolate (1.15–1.33) orprolate (1.34- 2.00). Descriptive analysis of pollen morphometrics was performed, and Duncan’s multiple range test was used to investigate the differences between the genotypes. The possibility of pollen selection was analyzed using a frequency distribution superimposed on the expected Gaussian distribution (D’Agostino test). The genetic divergence among the genotypes was quantified by D² values using Mahalanobis D² statistics [24] based on Tocher’s method and the R package “biotools” [25].

The results from detailed scanning electron microscopy images processed using FijiJ software revealed that most of the African marigold pollen grains belonged to the oblate spheroidal group, followed by the suboblate and rarely oblate groups, according to the classification of [23] (Fig. 1). The pollen grains of the marigold plants were isopolar and radially symmetrical with tricolpi apertures. The spines on the walls of the pollen grains were pyramidshaped and often conical, with a wide base at the bottom and a blunt to pointed apical tip.

Descriptive statistics for pollen morphometrics were calculated to determine the general characteristic features of the marigold pollen grains (Table 2). The results revealed lower variance and range for all the traits under study, except for the perimeter of the pollen grains. The lengths of the polar and equatorial axes ranged from 22.64 to 39.57 µm and 25.31 to 49.74 µm, respectively, while the perimeter of the pollen grains ranged from 82.33 to 133.14 µm. Furthermore, the results revealed that the data pertaining to the polar axis followed a normal distribution, as the values obtained for skewness were near zero. In contrast, all the other traits studied had skewed distributions.

Table 2

General descriptive statistics of African marigold pollen grains
	Perimeter (µm)	P: Polar axis (µm)	E: Equatorial axis (µm)	Length of ectoaperture (µm)	P/E ratio
Mean	101.42	29.39	32.86	4.51	0.90
Range	82.33- 133.14	22.64–39.57	25.37–49.74	1.86–10.61	0.64–1.05
Sample Variance	93.39	9.36	11.74	2.79	0.01
Skewness	0.62	0.22	0.59	0.95	-0.91

Analysis of variance was used to assess the statistical significance of differences in pollen morphological traits among various flower forms of marigold. The results revealed significant differences among the different flower forms for the traits studied (Table 3). Petaloid male sterile flowers exhibited significantly greater values for almost all the traits than did the other flower forms. The semidouble fertile form displayed the lowest values for perimeter and both polar and equatorial axis lengths. Petaloid male sterile flowers were found to be on par with the double-fertile form for the equatorial axis and the apetaloid double-fertile and double-fertile form for the polar axis. Furthermore, Duncan’s multiple range test was used to analyze the relationships and differences between the genotypes. Significant variations were observed for all the traits among the genotypes (Table 4). The genotype IIHRM 2–3 SF was significantly different for most of the traits under study except for the equatorial axis. The genotype IIHRMO 2330 was significantly different in terms of the trait perimeter of the pollen grains. Across the genotypes, the trait P/E ratio did not vary significantly. The pollen grains, classified according to Edrtman’s classification, revealed three shapes: oblate spheroidal, suboblate and rarely oblate. Moreover, across the genotypes, oblate spheroidal-shaped pollen grains were dominant, followed by suboblate pollen grains.

Table 3

Pollen morphometric features of different flower forms in African marigolds
Flower forms	Perimeter (µm)	P: Polar axis (µm)	E: Equatorial axis (µm)	Length of ectoaperture (µm)	P/E ratio
Single fertile	101.26^b	28.26^c	32.70^b	4.86^b	0.87c
Semidouble fertile	92.04^d	27.35^c	30.21^d	5.14^b	0.91b
Double fertile	103.62^b	30.18^b	34.09^a	3.88^c	0.89bc
Apetaloid sterile with single fertile	96.54^c	27.54^c	30.64^cd	3.72^c	0.90bc
Apetaloid sterile with double fertile	96.25^c	30.39^b	31.92^bc	3.75^c	0.95^a
Petaloid sterile with single fertile	114.55^a	32.16^a	35.26^a	6.36^a	0.91^b
F value	33.58*	17.27*	14.96 *	14.89 *	4.88 *
SE (m) ±	1.39	0.49	0.56	0.28	0.01
SE (d)	1.97	0.69	0.79	0.40	0.02
CD (1%)	5.11	1.78	2.03	0.78	0.05
(* p ≤ 0.01)

Table 4

Morphometric analysis of pollen grains from African marigold genotypes
Genotypes	Perimeter (µm)	P: Polar axis (µm)	E: Equatorial axis (µm)	Length of ectoaperture (µm)	P/E ratio	Shape of pollen
IIHRMO12	98.76 ^de	26.70^e	31.85^cd	6.36^a	0.84^e	Oblate spheroidal, suboblate and oblate
IIHRMO53	103.77^c	29.81^cd	33.54^b	5.15^b	0.89^bcd	Oblate spheroidal and suboblate
IIHRMO 2330	92.04^f	27.35^e	30.21^e	4.91^bc	0.91^bcd	Suboblate and oblate
IIHRMY 1–4	100.59^cd	29.02^d	33.37^bc	3.66^d	0.88^cde	Oblate spheroidal and suboblate
IIHRMO 2335	101.96^cd	30.10^bcd	32.58^bc	4.81^bc	0.92^ab	Oblate spheroidal
IIHRMY 2 − 1	108.32^b	31.40^ab	36.33^a	3.62^d	0.87^de	Oblate spheroidal, suboblate and oblate
IIHRMO 2356 SF	96.25^e	30.39^bcd	31.92^cd	3.81^d	0.95^a	Oblate spheroidal
IIHRMO 2337 SF	96.54^e	27.54^e	30.63^de	3.84^d	0.90^bcd	Oblate spheroidal and suboblate
IIHRM 2–3 SF	114.55^a	32.15^a	35.26^a	4.18^cd	0.91^abc	Oblate spheroidal, suboblate and oblate
SE (d) ±	1.89	0.65	0.75	0.41	0.02
CD 5%	3.72	1.28	1.47	0.80	0.04
*superscript letters denote grouping through Duncan Multiple Range test

Tocher’s method of D² statistics was used to estimate the genetic distance between the marigold genotypes belonging to the same flower form as well as other forms. For the investigation, whether the genotypes belonging to the same flower form were grouped together, the results indicated that the genotypes associated with all the traits studied were clustered into five distinct clusters (Table 5). Five genotypes that belonged to the double-fertile and semidouble fertile groups were grouped under the first cluster, whereas the remaining four genotypes were individually separated into four different clusters without exhibiting a definite trend.

Table 5

Mahalanobis distance between African marigold genotypes based on their pollen morphometric traits
	Cluster I					Cluster II	Cluster III	Cluster IV	Cluster V
	IIHRMO 2330	IIHRMO 2335	IIHRMY 1–4	IIHRMO 2356 SF	IIHRMY 2 − 1	IIHRMO 53	IIHRMO 2337 SF	IIHRMO 12	IIHRM 2–3 SF
IIHRMO 2335	9.16
IIHRMY 1–4	2.44	7.24
IIHRMO 2356 SF	10.79	3.65	9.29
IIHRMY 2 − 1	8.21	8.56	4.45	9.67
IIHRMO 53	6.30	11.53	8.98	8.36	14.71
IIHRMO 2337 SF	7.67	5.43	5.44	12.03	15.34	13.52
IIHRMO 12	13.44	8.99	10.42	15.16	11.07	10.63	12.02
IIHRM 2–3 SF	7.40	7.64	12.61	13.71	12.78	13.60	13.93	13.81	-

The variability observed for pollen morphological traits across the genotypes is represented in a box plot for each trait (Fig. 2). A symmetric distribution was recorded only for the polar axis, while an asymmetric distribution was recorded for all the other traits for all the genotypes. The IIHRM 2–3 SF genotype exhibited the highest variability for all the traits under study, followed by the IIHRMO 2330 variety, and the lowest variability was observed for the IIHRMO 2356 SF genotype. Furthermore, for the trait polar and equatorial axis genotype IIHRMO 2330, outliers were recorded, although the range of variability was narrower.

The observed frequency distribution for pollen traits was found to deviate from the expected normal distribution, confirming the results revealed by the box plot. Instead of a single population normally distributed above the mean, two groups were observed within the pollen population of a single genotype distributed over two different mean values for the polar and equatorial axes, suggesting the possibility of pollen selection. Two groups of IIHRMY1-4 and IIHRMO 2337 SF were observed for the equatorial axis, while two groups of IIHRMO 2330 and IIHRM 2–3 SF were observed for the polar axis, revealing variability within the genotypes (Fig. 3).

Pollen studies help researchers understand the systematic and evolutionary relationships of various groups of flowering plants [27], and in the Asteraceae family, studies have confirmed that pollen morphological characteristics are useful tools for taxonomic classification [28]. The goal of the present study was to study the characteristic features of African marigold plants and to understand the variability among the flower forms across the genotypes. Pollen grains of marigold were found to be more or less spheroidal, tricolporate, with conical pointed or blunt spines irregularly distributed on the pollen wall, which was similar to the characteristics reported in the Asteraceae family [11, 29, 30] and its tribe Coreopsidae[31]. The most dominant shape observed for marigold pollen grains was oblate spheroidal, followed by suboblate. Similar pollen shapes,viz. oblate-spheroidal plants were also recorded in Dahlia and Hidalgoa species, which belong to Asteraceae [30], while Centaurea species, which also belong to the Asteraceae family, had prolate spheroidal shapes in their pollens [11],revealing the species-specific nature of the pollens.

Significant differences were observed among the different flower forms and genotypes for the traits studied; however, the relationship between the genotypes and the flower forms could not be easily established. The estimation of genetic diversity is crucial for identifying distinct genotypes. D² statistics are the easiest biometrical tool for identifying genetically similar and distinct genotypes and could be useful in future breeding programs. Based on the results obtained from Tocher’s method, five distinct clusters were formed based on all the pollen morphological traits, with the maximum number of genotypes occurring in the first cluster, and all the genotypes were found to be double fertile. Thus, all the double types of fertile flowers, including those with a fertile counter to apetaloid sterile types, exhibited similar pollen morphologies. In contrast, the genotypes belonging to the single fertile group or sterile forms where the fertile flowers were of single types did not form a single cluster. Thus, the analysis did not strictly categorize the genotypes based on their flower forms. In contrast, using a similar method, Magdalena [12], were able to group Linum usitatissimum genotypes based on their utility.

The results obtained from the box plot showed variation across the genotypes, while frequency distribution studies revealed variation within the genotype. Furthermore, the size of the pollen grain is the critical factor that determines the success of pollination and is influenced by postpollination male–male competition [32].The polar and equatorial axes determine pollen grain size, and for these traits, deviation from a normal distribution within the genotype was observed, indicating the possibility of gametophytic selection, a breeding approach wherein a particular trait can be selected in its haploid state that prevents dominant alleles from concealing recessive alleles [33]. In majority of the genotypes under investigation, a greater number of genotypes with longer polar and equatorial axes were found. These differences are crucial to breeding efforts because they increase the prospect of pollen selection within the population. Earlier studies have demonstrated the success of gametophytic selection in breeding different crops for various characteristics[19,20, 34, 35, 36].

The palynological description reported here is significant for advancing our knowledge of reproductive biology in African marigolds. The characteristic features of African marigold pollen grains are an isopolar monad mostly oblate-spheroidal in shape, with three colpi and sharp to blunt spines on the pollen walls. Significant variability was observed across the flower forms and within the genotype. Deviations from the normal distribution for traits such as polar and equatorial axes, which determine the shape and size of the pollen grains, suggest the possibility of gametophytic selection within the genotype for crop improvement programs in marigolds. The variability observed for pollen traits across the genotypes and flower forms suggests the possibility of exploring similar studies in many other commercially important species. An elaborate study of pollen wall ornamentation and exine thickness and its relationship with pollen grain vigor and germination may further help in the assessment of the inter- and intraspecific variability of the use of pollen wall ornamentation in hybrid seed development.

Compliance with Ethical Standards

Data availability statements

All the data generated and analyzed during this study are included in this manuscript.

Conflict of interest

The authors declare that there are no conflicts of interest. The authors also declare that the manuscript has neither been submitted nor is under consideration for publication elsewhere. All the authors have read and commented on the manuscript.

Funding

No funding was received to assist with the study and preparation of this manuscript.

Author Contributions

PT conceived and designed the experiment. LD performed the experiments, LD and VP assisted SD for imaging the marigold pollen grains in SEM. LD analyzed the data with assistance from PT and RV. LD wrote the draft manuscript under guidance of PT. All the authors discussed the results and commented on the manuscript.

Ethics Declaration

Ethics approval and consent to participate

The plants used in the study is owned to the breeder who generated them who is Dr. Tejaswini Prakash (one of the authors) who is the Principal Scientist and handling the breeding work in marigold at ICAR-Indian Institute of Horticultural Research, Bengaluru India, where the study has been conducted. Therefore, the collection of plants used in the study complies with the local and national guidelines with no need for further affirmation. This article does not contain any studies with human participants or animals performed by any of the authors.

Acknowledgments

The first author acknowledges the Head of the Division of Crop Protection for providing the necessary Scanning Electronic Microscope facility for successful imaging of the marigold pollen grains.

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Can flower forms be indicators of pollen diversity and possible gametophytic selection in marigold breeding programs?

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