Evidence of maternal effect on the inheritance of flax (Linum usitatissimum L.) seed coat color

Abstract

This study aimed to investigate the presence of maternal effect on the inheritance of flax seed coat color. Direct and reciprocal crosses were performed between four yellow flax seed lines and two brown flax seed cultivars. F₁ and F₂ populations of direct and reciprocal crosses were evaluated for coat color. Four F₂ populations were selected for analysis of coat color in the F₃ generation. The phenotypic segregation pattern was assessed by the chi-square test. The nuclear genotype of the female parent influenced all F₁, F₂, and F₃ populations. F₁ and F₂ seeds were always equal to the phenotype of the female parent. F₃ populations had a 3:1 ratio of plants producing yellow and brown seeds. The maternal effect resulted from the transfer of gene products from maternal cytoplasm to offspring, with evidence of the effect of a single gene with a dominant allele for the yellow phenotype.

Keywords:
Chi-square test; genetic improvement; female parent; reciprocal cross

INTRODUCTION

Flax or linseed (Linum usitatissimum L.) is an autogamous, diploid (2n = 2x = 30 chromosomes), annual winter plant (Allaby 2005). The plant can be used for the production of textile fibers, and its seeds can be used in human and animal nutrition and, mainly, for the extraction of flax seed oil, which is an important raw material in the chemical industry (Dal’Coll Lúcio et al. 2021). Given its high content of linolenic acid, flax seed oil is susceptible to oxidation and polymerization, serving as an excellent drying agent for paints, varnishes, dyes, waxes, synthetic leather, and linoleum floors, among others (Dash et al. 2017, Parikh et al. 2019). Furthermore, the seed is rich in omega-3 and -6 fatty acids, protein, and digestible fiber. Raw flax seeds, flax seed flour, and flax seed meal constitute healthy additions to the human diet and may contribute to disease prevention. Flax seed oil and meal are also added to animal diets as energy sources (Singh et al. 2011, You et al. 2016).

Seed color is an important attribute influencing the market value of flax cultivars. This trait is mainly determined by the concentration, composition, and polymerization degree of tannins in outer coats (Bangar et al. 2021, Tomaszewska-Gras et al. 2021). Seed coat color in flax can range from yellow, olive, light brown, or dark brown (Diederichesen and Raney 2008) to variegated (Mitappali and Rowland 2003). Yellow flax seeds have thin and soft hulls. This coat color results from inhibition of the biosynthesis of proanthocyanidins, condensed tannins that impart a brown color to the seed coat (Kajla et al. 2015, Xu et al. 2015) and serve as a valuable source of antioxidants. It should be noted that, although yellow seeds do not contain tannins, their cotyledons are rich in carotenoids (Troshchynska et al. 2019).

Studies showed that yellow-seed genotypes had lower seed yield, attributed to the lower vigor, lower germination rate, and lack of flavonoids in yellow seeds (Saeidi and Rowland 1999, Zare et al. 2021, Abtahi et al. 2022). Abtahi et al. (2022) argued that red or brown seed colors may serve as effective markers for the indirect selection of oil- and protein-rich genotypes. Because of the importance of seed color in the export market, this trait is included in all flax breeding programs (Mittapali and Rowland 2003, Sudarshan et al. 2017, Zare et al. 2021, Abtahi et al. 2022).

In flax, seed coat color is controlled by three (Tammes 1922, Barnes et al. 1960, Comstock et al. 1969) or four nuclear loci (Mittapalli and Rowland 2003). The Y1 allele confers a dominant yellow color to the seed coat, whereas alleles g, d, and b1 confer a recessive yellow color. In these cases, the alternative phenotype is always brown. There is also a recessive allele for the b1 locus, which is called b1^vg because its expression produces a variegated seed coat (Saeidi and Rowland 1997). None of the previous studies reported the maternal effect on flax seed coat color.

The maternal effect is defined as the causal influence of the maternal genotype or phenotype on the offspring phenotype. Maternal genetic effects occur when genes present in the mother's genome affect the phenotype of her offspring (Wolf and Wade 2009). Many of the known maternal effect genes act via maternal mRNA or proteins (Berleth et al. 1988, Tong et al. 2000) that coordinate development, particularly prior to the maternal-to-zygotic transition, and often represent products from the majority of the genes in the genome (Baroux et al. 2008).

This study aimed to investigate the presence of maternal effect on the inheritance of flax seed coat color using direct and reciprocal crosses of yellow-seed lines and brown-seed cultivars.

MATERIAL AND METHODS

F₁, F₂, and F₃ generations were produced by crossing contrasting genotypes for flax seed coat color. Two brown-seed cultivars and four yellow-seed lines of flax were used. The brown-seed cultivars were Caburé and Aguará, both from the National Institute of Agricultural Technology (INTA) of Argentina. The yellow-seed lines were LIN49, LIN57, LIN88, and LIN36, obtained from a Brazilian genetic improvement program. All genotypes have violet-blue flowers.

The study was carried out in 2020 and 2021 at the Center for Rural Sciences of the Federal University of Santa Catarina, Curitibanos (lat 27° 16’ 34” S, long 50° 30’ 12” W, alt 1040 m asl, Cambisol, average annual precipitation of 1500 mm), Santa Catarina State, Brazil, and in 2022 at the Francisco Beltrão Campus of the Federal University of Technology - Paraná (lat 24° 05’ 37” S, long 53° 05’ 64” W, alt 553 m asl, Ferralsol, average annual precipitation of 1700 mm), Paraná State, Brazil.

In 2021, seeds from the four lines and two cultivars were sown in pots in a greenhouse. For synchronized flowering, cultivars were sown earlier than lines. Crosses were made with the plants in full bloom. Emasculation was performed in the late afternoon. Pollination was performed in the morning by placing an anther with pollen on the tip of the stigma of an emasculated flower. Sixteen F₁ populations were obtained, as described in Table 1.

Table 1
Direct and reciprocal crosses between yellow-seed lines and brown-seed cultivars of flax

Maternal progenitor ♀		Paternal progenitor ♂	Seed phenotype	No. crossed flowers	Seeds/capsule
LIN49	×	Aguará	yellow × brown	4	6
Aguará	×	LIN49	brown × yellow	14	9
LIN49	×	Caburé	yellow × brown	11	7
Caburé	×	LIN49	brown × yellow	8	5
LIN57	×	Aguará	yellow × brown	10	7
Aguará	×	LIN57	brown × yellow	15	6
LIN57	×	Caburé	yellow × brown	11	7
Caburé	×	LIN57	brown × yellow	9	7
LIN88	×	Aguará	yellow × brown	11	7
Aguará	×	LIN88	brown × yellow	10	8
LIN88	×	Caburé	yellow × brown	16	8
Caburé	×	LIN88	brown × yellow	9	7
LIN36	×	Aguará	yellow × brown	16	5
Aguará	×	LIN36	brown × yellow	15	8
LIN36	×	Caburé	yellow × brown	15	5
Caburé	×	LIN36	brown × yellow	7	4

The coat color of F₁ seeds from all crosses was evaluated individually and recorded. In 2021, 10 seeds of each F₁ population were sown under field conditions in Curitibanos, Santa Catarina, Brazil. This procedure was used to obtain F₁ plants and F₂ seeds, the latter of which were produced by natural self-pollination. At maturity, all F₁ plants were harvested individually, and the coat color of F₂ seeds was evaluated and recorded. In 2022, F₂ seeds from four populations (LIN88 × Aguará, Aguará × LIN88, LIN88 × Caburé, and Caburé × LIN88) were sown under field conditions in Francisco Beltrão, Paraná, Brazil. At maturity, F₂ plants (100 plants per cross) were harvested individually, and the coat color of F₃ seeds was evaluated. Crop management was the same for both years. Seeds were sown at a spacing of 0.34 cm. Sowing, weeding, and harvesting were manual.

Observed values were compared with expected values within each F₃ population by a chi-square (χ ²) goodness-of-fit test at a significance level (alpha) of 0.05. Moreover, F₁, F₂, and F₃ populations were compared with their reciprocals. Statistical analyses were performed using GENES software (Cruz 1998).

RESULTS AND DISCUSSION

F₁ seeds had the same coat color phenotype within each direct and reciprocal cross. F₁ seeds resulting from crosses with LIN88 (yellow seeds) as the female parent and Aguará or Caburé (brown seeds) as the male parent showed a yellow phenotype. F₁ seeds from crosses in which the female parent was a brown-seed cultivar exhibited a brown phenotype. Therefore, in comparing direct and reciprocal crosses, it was observed that the phenotype of F₁ seeds was always equal to the phenotype of the female parent (Table 2), suggesting the existence of maternal effect on the coat color of flax seed. After F₁ plants were harvested and thrashed and F₂ seeds analyzed, it was found that, for all direct and reciprocal crosses, there was no segregation of flax seed color. All seeds were yellow (Table 2).

Table 2
Number of yellow and brown seeds produced by F₁ and F₂ generations from direct and reciprocal crosses between yellow-seed lines and brown-seed cultivars of flax

Maternal progenitor ♀	Paternal progenitor ♂	F1 seeds		F2 seeds*
		Yellow	Brown	Yellow	Brown
LIN49 (Y)	Aguará (B)	17	0	1000	0
Aguará (B)	LIN49 (Y)	0	96	1000	0
LIN49 (Y)	Caburé (B)	60	0	1000	0
Caburé (B)	LIN49 (Y)	0	44	1000	0
LIN57 (Y)	Aguará (B)	55	0	1000	0
Aguará (B)	LIN57 (Y)	0	62	1000	0
LIN57 (Y)	Caburé (B)	72	0	1000	0
Caburé (B)	LIN57 (Y)	0	51	1000	0
LIN88 (Y)	Aguará (B)	67	0	1000	0
Aguará (B)	LIN88 (Y)	0	84	1000	0
LIN88 (Y)	Caburé (B)	116	0	1000	0
Caburé (B)	LIN88 (Y)	0	51	1000	0
LIN36 (Y)	Aguará (B)	61	0	1000	0
Aguará (B)	LIN36 (Y)	0	97	1000	0
LIN36 (Y)	Caburé (B)	74	0	1000	0
Caburé (B)	LIN36 (Y)	0	17	1000	0

• Y, yellow; B, brown.
• * All plants from the F₂ generation were evaluated.

As shown in Table 3, F₃ seeds, originated from 100 F₂ plants from each cross, had the same 3:1 phenotypic segregation ratio of yellow to brown seeds, as confirmed by chi-square statistics. These findings indicate the presence of nuclear gene, containing two alleles under dominant allele interaction, with the dominant allele conferring the yellow and the recessive allele conferring the brow phenotype.

Table 3
Chi-square tests for goodness-of-fit of seed color in pooled F₂ populations for all classes of crosses used to study the inheritance of flax seed coat color

Maternal progenitor ♀	Paternal progenitor ♂	F2 plants and F3 seeds (number)		χ 2	p-value
		Yellow	Brown
LIN88 (Y)	Aguará (B)	72	28	0.48	0.48
Aguará (B)	LIN88 (Y)	70	30	1.33	0.25
LIN88 (Y)	Caburé (B)	75	25	0.0	1.00
Caburé (B)	LIN88 (Y)	73	27	0.21	0.64

• Y, yellow; B, brown.

Analysis of F₃ seeds is important for confirming the results of previous generations. A summary of the steps and phenotypic results of the study of the inheritance of flax seed coat color is also presented in Figure 1.

Figure 1
Schematic summary of the study of the inheritance of flax (Linum usitatissimum L.) seed coat color, with direct and reciprocal crosses, F₁ and F₂ populations (seeds and plants), and F3 population (seeds).

The results for F₂ and F₁ seeds were compared with those previously reported in the literature (Tames 1922, Shaw et al. 1931, Barnes et al. 1960, Mitappali and Rowland 2003, Sodi et al. 2012). The literature states that three or four genes control flax seed color, with possible epistasis between genes. In the vast majority of cases, the dominant allele is brown, with the exception of the dominant allele Y1, which confers a dominant yellow phenotype (Green and Dribnenki 1995, Popescu and Marinescu 1996). Previous studies showed that F₁ seeds from direct and reciprocal crosses exhibited the same color: in crosses between brown (dominant) and yellow (recessive) seeds, the color of resulting seeds was brown, owing to the heterozygous genotype of the embryo, indicating single-gene nuclear inheritance. However, the results of the current study are contrasting and showed that the maternal effect was responsible for the coat color of flax seed.

Maternal inheritance is a conceptually related set phenomenon associated with uniparental inheritance of organelle genomes, cytoplasmic elements, symbionts, substances, and factors, as well as parent-of-origin gene expression effects, and maternally controlled genomic imprinting. Although conceptually similar, the types of maternal inheritance have widely differing mechanisms, evolutionary and genetic consequences, and evolutionary and genetic consequences (Badyaev 2013). Inheritance of cytoplasmic genes occurs via the transfer of mitochondria and chloroplasts from the female gamete to offspring. By contrast, the mechanism for the maternal effect is generally through the maternally provided ‘environment’, whether in the form of maternal messenger RNAs and proteins that are pre-loaded into the unfertilized egg or ovule, or in the form of post-zygotic influences via maternal traits such as nutritional provision. When the maternal effect is determining the inheritance of a trait, there is a causal influence of the maternal genotype or phenotype on the offspring phenotype (Wolf and Wade 2009).

Therefore, the maternal effect does not arise due to units of heredity, but due to products of the maternal supply. In line with the maternal effect hypothesis, a possible explanation for our findings is that the F₂ seeds of the populations, despite having different genotypes, developed from genetically identical F₁ plants. Therefore, the yellow color of the seeds was a result of gene products present in the mother's cytoplasm, which were transmitted to the offspring.

Flax seed consists of three major tissues: the diploid embryo and triploid endosperm as products of double fertilization and the maternal seed coat tissue (Venglat et al. 2011). According to Miart et al. (2021), the color of flax seed coat varies during seed development before the mature coat is established, suggesting the existence of modifications in some seed coat-specific components, including phenolic compounds such as proanthocyanidins. Soon after fertilization, the seed is translucent. The thick, clear, fragile coat of the fertilized ovule differentiates into a thin, dark, protective seed coat during seed development (Venglat et al. 2011). This explains why, in many crops, although the seed coat is of maternal origin, the final phenotype of the offspring seed is not always the same as that of the mother plant, being determined by the genotype of the embryo resulting from fertilization. The maternal effect has been related to seed color in other crops, such as sesame (Laurentin and Benitez 2014), rapeseed (Zhi-wen et al. 2005), and common bean (Possobom et al. 2015). Maternal effects have also been observed on the fatty acid composition of soybean (Gilsenger et al. 2010) and common bean seed size and morphology (Singh et al. 2017).

Given that the phenotype of F₂ seeds is the result of the maternal nuclear genotype (heterozygous F₁ plants), it is suggested that the yellow seed phenotype was dominant over the brown seed phenotype. The dominance of the yellow seed phenotype has been reported in previous studies suggesting that the Y1 gene, independent of the aforementioned G, D, and B1 genes, is responsible for such dominance (Green and Dribnenki 1995, Popescu and Marinescu 1996, Mittapalli and Rowland 2003). Mittapalli and Rowland (2003) reported the presence of the Y1 gene in the yellow-seed cultivar Bionda from Germany.

The results converge on the hypothesis of the expression of a dominant allele (Y1) conferring yellow seeds to lines (here represented by LIN88) and a recessive allele (y1) conferring brown seeds to cultivars Aguará and Caburé. To improve the understanding of the results, we adopted the following genotypic identification: LIN88 = Y1Y1, Aguará and Caburé = y1y1. It was considered that all yellow lines had the same genotype for the Y1 gene, given that they were from the same selection of plants that originated the LIN88 line. Likewise, both cultivars, originating from the same breeding program, were considered to have the same genotype, as supported by the results. Figure 2 presents a synthesis of our results, including seed phenotype and the genotypic composition of each population.

Figure 2
Model explaining maternal effect on flax seed coat color inheritance based on direct and reciprocal crosses and F1, F2 and F3 generations. Genotypes and phenotypes are presented, considering the Y1 gene.

Direct and reciprocal crosses of yellow seed lines (Y1Y1) with brown seed cultivars (y1y1) resulted in F₁ seeds with the phenotype of the female parent, which led to different phenotypes in direct and reciprocal crosses (Table 2 and Figure 2). Although F₁ seeds from direct and reciprocal crosses showed the same nuclear genome (Y1y1), flax seed color resulted from the maternal genotype, as the cytoplasmic genome was different. Because flax is an autogamous plant (Hall et al. 2016) and F₁ plants are self-pollinated, it would be expected that F₂ seeds had the same genotypic segregation ratio of a nuclear gene with two alleles (1:2:1). However, F₂ seeds also exhibited the phenotype resulting from the maternal nuclear genotype (F₁ plants, Y1y1), being 100% yellow (Table 2 and Figure 2).

Natural self-pollination of F₂ plants generated F₃ seeds, had a 3:1 phenotypic segregation of yellow to brown seeds, respectively (Table 3 and Figure 2). In segregating populations such as those of F₂ plants, which gave origin to F₃ seeds, 50% of plants are expected to be homozygous (1/4 dominant and 1/4 recessive) and 1/2 heterozygous. Each homozygous F₂ plant was expected to produce a homogeneous offspring regarding the color (F₃ seeds), without segregation for color. Dominant homozygous plants generated yellow seeds and recessive homozygous plants generated brown seeds. Heterozygous F₂ plants, on the other hand, were expected to produce segregating F₃ seeds: 1/2 homozygous (1/4 dominant and 1/4 recessive) and 1/2 heterozygous. Therefore, after two generations of self-fertilization, the F₃ population was expected to be composed of 3/8 homozygous dominant yellow seeds, 1/4 heterozygous yellow seeds, and 3/8 homozygous recessive brown seeds. However, we observed a 3:1 phenotypic segregation (75% yellow and 25% brown), because F₃ seeds expressed the phenotype of the F₂ maternal genotype. F₃ seeds from heterozygous F₂ plants did not show segregation; all seeds were yellow, which was the dominant phenotype. In fact, none of these plants produced seeds with phenotypic segregation (Figure 2). A phenotypic segregation of 5/8 yellow seeds to 3/8 brown seeds is expected to be expressed in F₄ seeds.

The proposed model explains the maternal genotype effect on the inheritance of flax seed coat color, suggesting the presence of the Y1 gene (Green and Dribnenki 1995, Popescu and Marinescu 1996, Mittapalli and Rowland 2003) in the germplasm of yellow lines. These lines are likely similar for the color genotype to the cultivar Bionda from Germany and the introduction CPI84495 from Australia, which exhibit dominance of yellow coat (Green and Dribnenki 1995, Popescu and Marinescu 1996).

Our results differ from those of previous studies with flaxseed. Mitappali and Rowland (2003) carried out an extensive study of flaxseed seed coat color, with genotypes from different germplasms, showing brown, yellow and even variegated (yellow parts and brown parts) seed phenotypes. However, even with a wide variety of genotypes, the authors do not report on the inheritance of maternal effect on flax seed coat color. Therefore, the absence of genetic studies with germplasm of flax cultivated in South American countries such as Brazil and Argentina was the motivation of this research.

The results reported here add a new facet to our understanding of the inheritance of flax seed color, describing for the first time the effect of the maternal genotype. These findings complement previous studies by providing evidence that the genetic background of parents is relevant to the inheritance of flax seed color, suggesting that this trait has more than one mode of inheritance. The results of studies on the inheritance of flax seed coat color should be considered in genetic breeding programs, as seed color influences the market value of flax seed. Additionally, flax seed color is related to several yield parameters and the physical and nutritional quality of seeds (Sudarshan et al. 2017, Zare et al. 2021, Abtahi et al. 2022)

CONCLUSION

The nuclear genotype of the female parent was responsible for flax seed coat color in crosses of Brazilian lines with Argentine cultivars. The maternal effect resulted from the transfer of gene products from maternal cytoplasm to offspring. The germplasm showed a single dominant gene with the yellow phenotype dominant and the brown phenotype recessive.

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Publication Dates

• Publication in this collection
  14 Aug 2023
• Date of issue
  2023

History

• Received
  27 Feb 2023
• Accepted
  01 June 2023
• Published
  28 June 2023