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. 2021 Mar 13;7(3):e06483. doi: 10.1016/j.heliyon.2021.e06483

Mapping chromosomal regions associated with anther indehiscence with exerted stigmas in CRI-48 and Jasmine 85 cross of rice (Oryza sativa L)

Samuel Oppong Abebrese a,∗, Nana Kofi Abaka Amoah b, Paul Kofi Ayirebi Dartey c, Isaac Kofi Bimpong b, Richard Akromah d, Vernon Edward Gracen e, Samuel Kwame Offei e, Eric Yirenkyi Danquah e
PMCID: PMC7973294  PMID: 33763616

Abstract

Anther indehiscence in certain wide crosses combines male sterility with stigma exertion, a phenomenon that is desirable for hybrid rice seed production. This study sought to identify chromosomal region(s) that combine anther indehiscence with exerted stigmas. A mapping population consisting of 189 BC1F1 plants was derived from a cross between CRI-48 and Jasmine 85 and backcrossing the resulting F1 to Jasmine 85. Contrary to the three complementary genes mode of inheritance reported earlier, a single locus (AI6-1) was mapped on chromosome 6 at 27.4 cM for anther indehiscence with exerted stigmas through a mixed model-based composite interval mapping (MCIM). This locus was flanked by two single nucleotide polymorphism (SNP) markers, K_ID6002884 and K_ID6003341 within a range of 23.1–28.9 cM. The allele at the locus was contributed by the CRI-48 parent which has Oryza glaberrima ancestry. This locus is suggested to control anther indehiscence and stigma exertion through pleiotropic gene action or cluster of genes.

Keywords: Outcrossing, Genetic mapping, Hybrid rice seed production, SNP markers, Pleiotropic gene action

Outcrossing, genetic mapping, hybrid rice seed production, SNP markers, pleiotropic gene action.

1. Introduction

Rice (Oryza sativa L.) is a major staple food crop in the developing world (Guimaraes, 2009; Seck et al., 2012). It is cultivated on 11% (156 million ha) of the world's total arable land second only to wheat in terms of harvested area (FAO, 2017). The demand for rice globally, is predicted to increase as a result of increased growth in population (IRRI, 2010; Seck et al., 2013; Muthayya et al., 2014). Khush (2005) estimates that global production will have to increase by 40% by the year 2030 to meet the growing demand for rice. Genetic improvement of rice has led to significant yield increases; however, average yields of inbred varieties have reached a plateau making further increments difficult (Khush, 2005; IRRI, 2010; Khan et al., 2015). Hybrid technology which exploits the phenomenon of heterosis presents a viable means of significantly increasing rice yield than the semi-dwarf inbred varieties currently being utilised (IRRI 1997; Guimaraes, 2009; Fischer et al., 2014; Khan et al., 2015).

Rice, being a strictly self-pollinating crop requires the use of a male sterility system to develop commercial hybrid varieties (Virmani, 1994; Virmani et al., 2003). Cytoplasmic male sterility (CMS) and environment-conditioned genetic male sterility (EGMS) are the two male sterility systems currently available for hybrid rice seed production. The extent and scope of outcrossing determine the ability of these male sterility systems to increase the efficiency of hybrid seed production. Earlier studies have indicated that efficiency of cross pollination in rice is influenced by floral traits including flowering behaviour, pollen longevity, stigma exertion and spikelet opening angle (Virmani, 1994; Takano-Kai et al., 2011). Among these, stigma exertion is the most important trait since it is directly involved in pollination (Virmani, 1994; Takano-Kai et al., 2011; Lou et al., 2014; Bakti and Tanaka, 2019; Xu et al., 2019).

Anther indehiscence, resulting from certain wide crosses, has been suggested as a form of functional male sterility (Sano, 1986; Oka, 1991; Maekawa et al., 1997; Dartey, 2007; Abebrese et al., 2018) with different modes of inheritance (Cheng and Huang 1980; Sano, 1986; Tamaru, 1991; Maekawa et al., 1997; Dartey, 2007). It has been found to combine male sterility with stigma exertion in specific crosses, a phenomenon believed to adapt the indehiscent plants to outcrossing (Dartey, 2007; Abebrese et al., 2018). This unique combination of anther indehiscence and stigma exertion could present a perfect male sterility system for hybrid rice seed production. The exerted stigmas would trap more pollens from the male parent thereby reducing the pollination barrier often encountered with some cytoplasmic male sterile lines and would increase hybrid seed set (Virmani, 1994; Takano-Kai et al., 2011).

Recent advances in molecular marker technology through quantitative trait loci (QTL) analysis, allow the identification of chromosomal region(s) underlying important traits in plants (McCouch and Doerge, 1995; Young, 1994; Toure et al., 2000; Collard et al., 2005; Jones et al., 1997, 2009; Nadeem et al., 2018). Breeders can get an insight into the number of loci controlling a trait, their relative importance and approximate positions in the genome (Jones et al., 1997, 2009; Breseghello and Coelho, 2013; Nadeem et al., 2018). Several marker systems are currently available for QTL mapping in plants (Semagn et al., 2006; Collard et al., 2008; Jones et al., 2009; Nadeem et al., 2018). Among these, single nucleotide polymorphism (SNP) markers have emerged as the marker of choice due to their low assay costs, high genomic abundance, locus-specificity, co-dominant inheritance, potential for high throughput analysis and relatively low rates of genotyping error (Semagn et al., 2006, 2014; McCouch et al., 2010, 2013). The continuous progress in high-throughput genomic technologies has led to numerous SNP genotyping platforms that combine a variety of chemistries and allele discrimination techniques (Semagn et al., 2014; Nadeem et al., 2018). Among these is the kompetitive allele specific PCR (KASP) (LGC group); a homogenous fluorescence-based genotyping variant of polymerase chain reaction which works based on allele-specific oligo extension and fluorescence resonance energy transfer for signal generation. This has emerged as a more flexible and cost-effective technique with minimal rate of genotyping error (Collard et al., 2008; Semagn et al., 2014; Smith and Moughan, 2015; Steele et al., 2018; Yang et al., 2019).

Over 20 genes have been reported to be involved in regulating anther dehiscence in plants (Keijzer, 1987; Goldberg et al., 1993; Matsui et al., 1999; Ma, 2005; Kobayashi et al., 2011; Wilson et al., 2011; Zhou et al., 2011; Peng et al., 2013; Ling et al., 2015; Cardarelli and Costantino, 2018; Estornell et al., 2018; Moon and Jung, 2020). For rice, Zhu et al. (2004) mapped anther indehiscence gene (aid1) on chromosome 6 using a two-element iAc/Ds transposon-tagging system. Using a similar approach, Thangasamy et al. (2011) also found that rice SUMO E3 ligase (siz1) gene on chromosome 5 controls spikelet fertility through regulation of anther dehiscence. Anther indehiscence in these two studies (Zhu et al., 2004; Thangasamy et al., 2011) was not associated with stigma exertion, but the genes had pleiotropic effect on other traits. Several studies have also mapped QTLs for stigma exertion on different rice chromosomes (Uga et al., 2003; Miyata et al., 2007; Yan et al., 2009; Li et al., 2014; Lou et al., 2014). Studies on the possible environmental effects on anther indehiscence with exerted stigmas suggested that light, temperature and relative humidity could not modulate the sterility/fertility status of anther indehiscence plants (Zhu et al., 2004; Abebrese et al., 2018; Estornell et al., 2018). Our earlier study (Abebrese et al., 2018) found three complementary genes mode of inheritance for anther indehiscence with exerted stigmas in the CRI-48/Jasmine 85 cross. Information on the chromosomal location of genes controlling anther indehiscence with exerted stigmas is currently lacking. Although it was previously not possible to employ nuclear controlled male sterility in hybrid rice seed production due to the inability to propagate a pure male sterile line, genetic engineering technique now allows constructing useable nuclear male sterile lines for hybrid rice seed production (Chang et al., 2016). Knowledge of the genes controlling anther indehiscence with exerted stigmas at the molecular level could help in manipulating the trait with advanced breeding techniques to develop a useable male sterility system with enhanced outcrossing for hybrid rice seed production. Therefore, as the first step, this study was carried out to identify chromosomal region(s) controlling anther indehiscence with exerted stigmas in a BC1F1 population of rice.

2. Materials and methods

2.1. Plant material

The parental materials used were two elite rice genotypes, CRI-48 (female) and Jasmine 85 (male). CRI-48 is an interspecific stabilized breeding line developed at the Council for Scientific and Industrial Research - Crops Research Institute (CSIR-CRI), Fumesua, Ghana, from the cross IDSA 85 × NERICA 1 (Figure 1). It has dehiscent anthers and non-exerted stigmas. Jasmine 85 is a fragrant indica variety which was developed at the International Rice Research Institute (IRRI) as IR841, from the cross IR262 × Khao Dawk Mali 105. It was released in the USA in 1989 as Jasmine 85 (Bollich, 1989; Asante, 2012). It was subsequently released as a commercial variety in Ghana in 2009 and for some time, was the most widely grown variety in Ghana because of its good taste, soft texture and fragrance (Asante et al., 2013; Ragassa et al., 2013). Jasmine 85 also has dehiscent anthers and non-exerted stigmas. The F1 progeny resulting from the cross between CRI-48 and Jasmine 85 exhibited anther indehiscence with exerted stigmas as observed in our previous study (Abebrese et al., 2018).

Figure 1.

Figure 1

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Pedigree of CRI-48 (CR-48 is a recombinant inbred line from IDSA 85 and NERICA1 cross. NERICA 1 is an interspecific line developed from WAB 56–104 (sativa-japonica) and CG 14 (glaberrima)).

2.2. Developing the mapping population

Jasmine 85 was crossed to CRI- 48 between July and October, 2013 at Nyankpala, Northern Ghana (090 24′ 17.8″ N, 000 0 57′ 57.0″ W, 143 m). The resultant F1 plants were raised in buckets. A single F1 plant was backcrossed to Jasmine 85 at the same location between July and October 2014. The 189 BC1F1 seeds were planted in buckets to raise 189 BC1F1 progenies which served as the mapping population for the present study (Figure 2).

Figure 2.

Figure 2

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Crossing scheme used to generate the BC1F1 mapping population: Jasmine 85 was crossed to CR-48 as the male parent to generate the first filial generation (F1), the F1 was backcrossed to Jasmine 85 to generate 189 seeds which were used to raise 189 individuals used as the mapping population.

2.3. Genotyping of the mapping population

Using a disc puncher, leaves (of 6mm diameter) were sampled from the two parents, four F1 plants and 189 BC1F1 plants three weeks after sowing and sent to LGC genomics, UK for DNA extraction and SNP genotyping. DNA extraction and KASP genotyping assay were carried out as described by Smith and Moughan (2015). The two parents were first screened with a total of 1885 SNP markers (LGC group) for polymorphism out of which 849 were polymorphic. Out of the 849 identified polymorphic markers, 246 evenly-spaced markers with known mapped positions were selected for genotyping the mapping population.

2.4. Phenotyping for anther indehiscence and stigma exertion

The phenotyping experiment was carried at Nyankpala, in the Guinea Savannah ecology of Northern Ghana (090 24′ 17.8″ N, 000 0 57′ 57.0″ W, 143 m). The seeds of the BC1F1 plants were pre-germinated in white tissue paper for four days and the resulting seedlings were nursed in buckets for 21 days followed by transplanting of one plant per 12 L bucket. Individual plants were provided with 8g of N.P.K. (15-15-15) fertilizer three weeks after transplanting, 4g of Ammonium sulphate at panicle initiation and watered whenever necessary. All other standard agronomic practices were followed as recommended. Individual plants were then phenotyped for the expression of anther indehiscence and stigma exertion. Dehiscence/indehiscence status of individual plants was scored by gently tapping panicles of individual plants at anthesis and visually observing extent of released pollen which was visible to the naked eye (Dartey, 2007). Absence of dehisced pollen was further checked with a hand lens to be sure that anthers remained indehiscent until drying up. Individual plants were scored for dehiscence/indehiscence of anthers and exerted/non-exerted of stigmas. Plants with dehiscent anthers and non-exerted stigmas were assigned zero (0) whereas their indehiscent counterparts with exerted stigmas were assigned one (1) for analysis.

2.5. Linkage map construction and QTL analysis

The genotyping data was used to construct a genetic linkage map for the CRI-48/Jasmine 85//Jasmine 85 BC1F1 population using QTL Network software v2.1 (Yang et al., 2007), a mixed model-based composite interval mapping (MCIM), based on default parameters of a 1000 permutation time, walk speed of 1cM, testing and filtration windows of 10cM each and a putative QTL detection at 0.05 significance level. MapChart Version 2.3 (Voorrips, 2002) was used for the construction of detailed linkage map showing the position of the QTL. The gene nomenclature followed that of McCouch et al. (1997) where a 2- or 3-letter abbreviation is followed by the number of chromosome on which the QTL is located and a terminal suffix, separated by a period, provides a unique identifier to distinguish multiple QTL on a single chromosome.

3. Results

3.1. Distribution of anther indehiscence and stigma exertion

The anther indehiscence trait was exhibited only by the F1s and subsequent generations of the CRI-48/Jasmine 85 cross but not their individual parents. Both CRI-48 and Jasmine 85 had dehisced anthers with non-exerted stigmas. All the F1 plants from the CRI-48/Jasmine 85 cross exhibited anther indehiscence with exerted stigmas (Figure 3). The BC1F1 plants segregated for anther dehiscence/indehiscence and stigma exertion/non-exertion. Out of the 189 BC1F1 plants scored for the mapping study, 38 had dehiscent anthers whereas 151 had indehiscent anthers (Table 1). Thirty-eight (38) plants had their stigmas not exerted whereas 151 plants had their stigmas exerted (Table 1). Florets with indehiscent anthers always had their stigmas exerted outside the hull whilst stigmas were enclosed within the hull for florets with dehiscent anthers (Table 1). The two parents also differed in many agro-morphological traits including days to flowering, basal pigmentation and grain length. Whereas Jasmine 85 flowered within 85 days, CRI-48 flowered at 70 days. The BC1F1 plants showed variations and segregated for the various agro-morphological traits. Temperature at flowering did not have any effect on the expression of anther indehiscence.

Figure 3.

Figure 3

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Anther indehiscence with exerted stigmas of the first filial generation (F1) between the CRI-48 and Jasmine 85 cross. Anthers fail to shed pollen till they wither (A). Stigmas exert outside the floret after indehiscent anthers wither (B).

Table 1.

Anther indehiscence and stigma exertion status of BC1F1 plants.

Plant No. Anther dehiscence status Stigma exertion status Plant No. Anther dehiscence status Stigma exertion status Plant No. Anther dehiscence status Stigma exertion status Plant No. Anther dehiscence status Stigma exertion status
Plant 1 Dehisce Non exerted Plant 26 Dehisce Non exerted Plant 51 Indehisce Exerted Plant 76 Indehisce Exerted
Plant 2 Indehisce Exerted Plant 27 Dehisce Non exerted Plant 52 Indehisce Exerted Plant 77 Dehisce Non exerted
Plant 3 Indehisce Exerted Plant 28 Indehisce Exerted Plant 53 Dehisce Non exerted Plant 78 Indehisce Exerted
Plant 4 Dehisce Non exerted Plant 29 Indehisce Exerted Plant 54 Indehisce Exerted Plant 79 Indehisce Exerted
Plant 5 Indehisce Exerted Plant 30 Dehisce Non exerted Plant 55 Indehisce Exerted Plant 80 Indehisce Exerted
Plant 6 Dehisce Non exerted Plant 31 Dehisce Non exerted Plant 56 Indehisce Exerted Plant 81 Indehisce Exerted
Plant 7 Indehisce Exerted Plant 32 Indehisce Exerted Plant 57 Indehisce Exerted Plant 82 Indehisce Exerted
Plant 8 Indehisce Exerted Plant 33 Indehisce Exerted Plant 58 Dehisce Non exerted Plant 83 Indehisce Exerted
Plant 9 Indehisce Exerted Plant 34 Indehisce Exerted Plant 59 Indehisce Exerted Plant 84 Indehisce Exerted
Plant 10 Dehisce Non exerted Plant 35 Dehisce Non exerted Plant 60 Indehisce Exerted Plant 85 Indehisce Exerted
Plant 11 Indehisce Exerted Plant 36 Dehisce Non exerted Plant 61 Indehisce Exerted Plant 86 Indehisce Exerted
Plant 12 Indehisce Exerted Plant 37 Indehisce Exerted Plant 62 Dehisce Non exerted Plant 87 Indehisce Exerted
Plant 13 Indehisce Exerted Plant 38 Indehisce Exerted Plant 63 Indehisce Exerted Plant 88 Indehisce Exerted
Plant 14 Indehisce Exerted Plant 39 Dehisce Non exerted Plant 64 Indehisce Exerted Plant 89 Indehisce Exerted
Plant 15 Indehisce Exerted Plant 40 Indehisce Exerted Plant 65 Indehisce Exerted Plant 90 Indehisce Exerted
Plant 16 Indehisce Exerted Plant 41 Indehisce Exerted Plant 66 Dehisce Non exerted Plant 91 Indehisce Exerted
Plant 17 Indehisce Exerted Plant 42 Indehisce Exerted Plant 67 Indehisce Exerted Plant 92 Indehisce Exerted
Plant 18 Indehisce Exerted Plant 43 Indehisce Exerted Plant 68 Indehisce Exerted Plant 93 Indehisce Exerted
Plant 19 Indehisce Exerted Plant 44 Dehisce Non exerted Plant 69 Indehisce Exerted Plant 94 Indehisce Exerted
Plant 20 Indehisce Exerted Plant 45 Indehisce Exerted Plant 70 Indehisce Exerted Plant 95 Indehisce Exerted
Plant 21 Dehisce Non exerted Plant 46 Indehisce Exerted Plant 71 Indehisce Exerted Plant 96 Dehisce Non exerted
Plant 22 Indehisce Exerted Plant 47 Indehisce Exerted Plant 72 Indehisce Exerted Plant 97 Indehisce Exerted
Plant 23 Dehisce Non exerted Plant 48 Indehisce Exerted Plant 73 Indehisce Exerted Plant 98 Indehisce Exerted
Plant 24 Indehisce Exerted Plant 49 Dehisce Non exerted Plant 74 Indehisce Exerted Plant 99 Indehisce Exerted
Plant 25
 Indehisce
 Exerted
 Plant 50
 Indehisce
 Exerted
 Plant 75
 Indehisce
 Exerted
 Plant 100
 Indehisce
 Exerted
Plant No.
 Anther dehiscence status
 Stigma exertion status
 Plant No.
 Anther dehiscence status
 Stigma exertion status
 Plant No.
 Anther dehiscence status
 Stigma exertion status
 Plant No.
 Anther dehiscence status
 Stigma exertion status
Plant 101 Indehisce Exerted Plant 126 Indehisce Exerted Plant 151 Indehisce Exerted Plant 176 Indehisce Exerted
Plant 102 Indehisce Exerted Plant 127 Indehisce Exerted Plant 152 Indehisce Exerted Plant 177 Dehisce Non exerted
Plant 103 Indehisce Exerted Plant 128 Indehisce Exerted Plant 153 Indehisce Exerted Plant 178 Indehisce Exerted
Plant 104 Indehisce Exerted Plant 129 Indehisce Exerted Plant 154 Dehisce Non exerted Plant 179 Indehisce Exerted
Plant 105 Indehisce Exerted Plant 130 Indehisce Exerted Plant 155 Indehisce Exerted Plant 180 Indehisce Exerted
Plant 106 Dehisce Non exerted Plant 131 Indehisce Exerted Plant 156 Dehisce Non exerted Plant 181 Indehisce Exerted
Plant 107 Dehisce Non exerted Plant 132 Indehisce Exerted Plant 157 Dehisce Non exerted Plant 182 Dehisce Non exerted
Plant 108 Indehisce Exerted Plant 133 Indehisce Exerted Plant 158 Indehisce Exerted Plant 183 Indehisce Exerted
Plant 109 Indehisce Exerted Plant 134 Indehisce Exerted Plant 159 Indehisce Exerted Plant 184 Indehisce Exerted
Plant 110 Indehisce Exerted Plant 135 Dehisce Non exerted Plant 160 Indehisce Exerted Plant 185 Indehisce Exerted
Plant 111 Indehisce Exerted Plant 136 Indehisce Exerted Plant 161 Indehisce Exerted Plant 186 Indehisce Exerted
Plant 112 Dehisce Non exerted Plant 137 Indehisce Exerted Plant 162 Dehisce Non exerted Plant 187 Indehisce Exerted
Plant 113 Indehisce Exerted Plant 138 Dehisce Non exerted Plant 163 Indehisce Exerted Plant 188 Indehisce Exerted
Plant 114 Indehisce Exerted Plant 139 Indehisce Exerted Plant 164 Indehisce Exerted Plant 189 Dehisce Non exerted
Plant 115 Indehisce Exerted Plant 140 Indehisce Exerted Plant 165 Indehisce Exerted
Plant 116 Indehisce Exerted Plant 141 Indehisce Exerted Plant 166 Indehisce Exerted
Plant 117 Indehisce Exerted Plant 142 Indehisce Exerted Plant 167 Dehisce Non exerted
Plant 118 Dehisce Non exerted Plant 143 Dehisce Non exerted Plant 168 Indehisce Exerted
Plant 119 Indehisce Exerted Plant 144 Dehisce Non exerted Plant 169 Indehisce Exerted
Plant 120 Indehisce Exerted Plant 145 Indehisce Exerted Plant 170 Indehisce Exerted
Plant 121 Indehisce Exerted Plant 146 Indehisce Exerted Plant 171 Indehisce Exerted
Plant 122 Indehisce Exerted Plant 147 Indehisce Exerted Plant 172 Indehisce Exerted
Plant 123 Indehisce Exerted Plant 148 Indehisce Exerted Plant 173 Indehisce Exerted
Plant 124 Indehisce Exerted Plant 149 Indehisce Exerted Plant 174 Indehisce Exerted
Plant 125 Indehisce Exerted Plant 150 Indehisce Exerted Plant 175 Dehisce Non exerted
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3.2. Genetic analysis and QTL detection

A genetic linkage map with 12 linkage groups corresponding to the 12 gametic rice chromosomes was constructed, spanning a total length of 1520.2 cM at an average marker interval of 6.18 cM (Table 2) using 246 markers. Chromosome 1 was the longest (179.4 cM) and had 40 markers with an average marker density of 4.49 cM. Chromosome 9 spanned 98.6 cM and was the shortest with average marker density of 7.58 cM. Summary of marker positions on the genetic linkage map is presented in Table 2. A single locus (AI6-1) was mapped at 27.4 cM on chromosome 6 for anther indehiscence with exerted stigmas. This locus was flanked by K_ID6002884 and K_ID6003341 within a range of 23.1–28.9 cM (Table 3; Figure 4). The allele at this locus was contributed by the CRI-48 parent which has Oryza glaberrima ancestry (Table 3).

Table 2.

Summary of genetic linkage map for the 246 SNP markers.

Chromosome Length (cM) Number of SNP makers Average marker density (cM)
1 179.4 40 4.49
2 142 25 5.68
3 160.4 22 7.29
4 114.6 22 5.21
5 132.1 23 5.74
6 122.3 24 5.1
7 108 22 4.91
8 130.2 17 7.66
9 98.6 13 7.58
10 100.9 11 9.17
11 114.4 14 8.17
12
 117.3
 14
 8.38
Total/Average 1520.2 246 6.18
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Table 3.

Information on the locus identified for anther indehiscence with exerted stigmas.

Locus Chr. Interval position range A SE P-Value Source of allele
AI6-1 6 K_ID6002884-K_ID6003341 27.4 23.1–28.9 -0.8388 0.0793 0.00001 CRI-48
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Figure 4.

Figure 4

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Genetic linkage map showing the locus (AI6-1) mapped for anther indehiscence with exerted stigmas on chromosome 6 between SNP markers K_ID6002884 and K_ID6003341.

4. Discussion

This study was set out to preliminarily map the chromosomal locations controlling anther indehiscence with exerted stigmas in rice for further studies on fine mapping and cloning the underlining gene (s). The underlying gene(s) could possibly be manipulated through marker assisted selection (MAS) or genetic engineering to develop male sterile rice lines with enhanced outcrossing for future hybrid rice seed production. The study followed the bi-parental mapping procedure.

Diverse parents are in vogue recommended for bi-parental QTL mapping studies to enable high marker polymorphism detection and adequate variation within the trait of interest (Collard et al., 2008; Jones et al., 1997, 2009). The presence of 849 polymorphic markers, representing 45% of the total 1885 SNP markers from the initial polymorphism survey suggests that the two parents were different in most of their genomic regions. This was likely because Jasmine 85 (the male parent) is an indica variety whereas the CRI-48 parent (the female parent) is from an interspecific japonica/NERICA cross with O. glaberrima parentage (Somado et al., 2008). A high-density genetic linkage map with evenly distributed markers is a prerequisite for identifying chromosomal regions that contain genes of interest using QTL analysis (McCouch and Doerge, 1995; Bernardo, 2008; Collard et al., 2008). A map length of 1520.2 cM generated from the 246 evenly distributed SNP markers was similar in length to linkage maps constructed using simple sequence repeat (SSR), restriction fragment length polymorphism (RFLPs) and amplified fragment length polymorphism (AFLPs) markers (Lanceras et al., 2000; Temnykh et al., 2000; Collard et al., 2008). An average marker density of 6.18 cM for the constructed map was appropriate for initial QTL detection. Bernardo (2008) recommended average marker density of <10 cM for such purposes.

Expression of anther indehiscence only by the F1s but not their individual parents suggests that the trait might be as a result of complementary genes from the two parents. Different modes of inheritance have been reported for anther indehiscence from different cross combinations (Sano, 1986; Maekaewa et al., 1997; Dartey, 2007). Our earlier study (Abebrese et al., 2018) found anther indehiscence with exerted stigmas in the CRI-48/Jasmine 85 cross to conform to the three complementary genes mode of inheritance reported by Dartey (2007). However, using genome-wide SNP markers, a single locus (AI6-1) was mapped for anther indehiscence with exerted stigmas in this current study. It could be that, the three complementary genes suggested by conventional genetic analysis are in a cluster. Fine mapping using denser molecular markers could reveal more in this direction. Segregation of anther indehiscence in the mapping population was skewed and did not fit into any of the earlier reported ratios (Sano, 1986; Maekawa et al., 1997; Dartey, 2007). Failure of the segregating pattern of the mapping population to conform to the 7:1 (indehiscence: dehiscence) mode of inheritance reported earlier could be due to the smaller population size. Also, hybridity of individual BC1F1 plants was mostly established by phenotypically examining the plants to confirm combination of unique traits of the two parents. Few plants which lacked such clear trait combinations were discarded. Such minor selection might have also contributed to the segregation distortion observed in the mapping population.

The locus for anther indehiscence with exerted stigmas in this study was mapped to 27.4 cM on chromosome 6. This locus was flanked by K_ID6002884 and K_ID6003341 within a marker interval of 23.1–28.9 cM Zhu et al. (2004) identified a rice (Oryza sativa L. cv Nipponbare) recessive mutant, anther indehiscence (aid1) gene, through the reverse genetics approach (a two-element iAc/Ds transposon-tagging system), showing partial to complete spikelet sterility. The aid1 gene which was mapped to 13.5 cM (124,000–140,000 bp) on chromosome 6 is about 13.9 cM away from the locus mapped in this present study. Among the several QTLs reported for stigma exertion of rice (Uga et al., 2003; Miyata et al., 2007; Yan et al., 2009; Lou et al., 2014), two (qPDES-6 and qPES-6) have been mapped on chromosome 6 (Lou et al., 2014). These two QTLs were flanked by simple sequence repeat (SSR) markers RM8225 and RM225 within an interval of 26.2–54.1 cM (3,416,523–9,309,118 bp, Nipponbare sequence 2009, www.gramene.org) on chromosome 6. The locus for anther indehiscence with exerted stigmas in this present study which was mapped within 23.1–28.9 cM is in the range reported by Lou et al. (2014). Florets with indehiscent anthers always had their stigmas exerted outside the hull whereas stigmas were enclosed within the hull for florets with dehisced anthers. Anther indehiscence always co-segregated with stigma exertion in a 964 BC1F1 segregating population reported by Abebrese et al. (2018) and that of a 517 reported by Dartey (2007). Therefore, it seems the single locus (AI6-1) controls anther indehiscence and stigma exertion pleiotropically. The aid1 gene reported by Zhu et al. (2004) had a pleiotropic effect on tillering and flowering time. Presence of pleiotropy could aid in manipulating the two traits together to design a useful male sterility system with enhanced outcrossing.

Review of literature suggests two sources of anther indehiscence genes. Anther indehiscence could originate from a single rice genotype or species (Cheng and Huang 1980; Sano, 1986; Li et al., 2011). For instance, Sano (1986) suggested a dominant gene (W020) from O. glaberrima as responsible for anther indehiscence. Cheng and Huang (1980) also traced anther indehiscence genes to O. rufipogon. Alternatively, anther indehiscence could also be as a result of complementary action of genes from two genotypes or species (Maekaewa et al., 1997; Dartey, 2007). Maekaewa et al. (1997) suggested that anther indehiscence is controlled by complementary action of three dominant genes. In their study, cv. Silewah (one of the parents for their mapping population) putatively had one of the three genes and cv. Hayakogane (the other parent) had the other two. Dartey (2007) also postulated involvement of three complementary genes to control anther indehiscence. Anthers dehisce if all three genes exist in the homozygous state, but indehiscence would result if one, two or all three genes exist in the heterozygous state. The allele at the mapped locus for this current study was contributed by the CR-48 parent. The CRI-48 has a glaberrima ancestry from its NERICA parent. The source of the anther indehiscence gene(s) could possibly be traced to this glaberrima parent. Anther indehiscence has also been reported as a common phenomenon in glaberrima-sativa crosses and was attributed to chromosomal aberrations (Sano, 1986).

5. Conclusion

The study identified a single mapped locus between SNP markers K_ID6002884 and K_ID6003341 on chromosome 6 for anther indehiscence with exerted stigmas. The allele at this locus was contributed by the CRI-48 parent which has Oryza glaberrima ancestry. We suggest that this locus controls anther indehiscence and stigma exertion through pleiotropic gene action or the three complementary genes might be in a cluster. Fine mapping with denser molecular markers could help uncover the underlying gene(s).

Declarations

Author contribution statement

Samuel Oppong Abebrese: Conceived and designed the experiments; Performed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data; Wrote the paper.

Nana Kofi Abaka Amoah: Performed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data; Wrote the paper.

Paul Kofi Ayirebi Dartey: Conceived and designed the experiments; Performed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data.

Isaac Kofi Bimpong: Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data.

Richard Akromah: Conceived and designed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data.

Vernon Edward Gracen; Samuel Kwame Offei; Eric Yirenkyi Danquah: Conceived and designed the experiments; Contributed reagents, materials, analysis tools or data.

Funding statement

This work was supported by Alliance for a Green Revolution in Africa (AGRA) through the West Africa Centre for Crop Improvement (WACCI), University of Ghana

Data availability statement

Data included in article/supplementary material/referenced in article.

Competing interest statement

The authors declare no conflict of interest.

Additional information

No additional information is available for this paper.

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