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Article

Effects of Traditional Ethnic Minority Food Culture on Genetic Diversity in Rice Landraces in Guizhou Province, China

by
Chunhui Liu
1,2,†,
Yanjie Wang
2,†,
Aixia Jiao
3,
Xiaoding Ma
2,
Di Cui
2,
Xiaobing Li
3,
Bing Han
2,
Huicha Chen
3,
Renchao Ruan
3,
Dayuan Xue
1,* and
Longzhi Han
2,*
1
College of Life and Environmental Sciences, Minzu University of China, Beijing 100081, China
2
Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
3
Institute of Crop Germplasm Resources, Guizhou Academy of Agricultural Sciences, Guiyang 550025, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2022, 12(10), 2308; https://doi.org/10.3390/agronomy12102308
Submission received: 22 August 2022 / Revised: 19 September 2022 / Accepted: 21 September 2022 / Published: 26 September 2022
(This article belongs to the Special Issue Advances in Rice Physioecology and Sustainable Cultivation)
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Abstract

:
Ethnic minorities living in Guizhou Province, China, have produced numerous rice landraces that are rich in genetic variations. Studying the genetic diversity and population structure of rice landraces in Guizhou has therefore become a topic of great research interest. However, the influence of ethnic minorities and their traditional food cultures on rice landraces remains unclear. We analyzed the genetic diversity of 598 rice landraces using simple sequence repeat (SSR) markers. Furthermore, we analyzed the nucleotide variations between two similar populations collected during two different time periods using a single-nucleotide polymorphism (SNP) haplotype analysis of six unlinked nuclear loci. The three major results were as follows: (1) The genetic diversity index of rice landraces in six ecologically distinct rice farming zones of Guizhou Province was high (He = 0.7721), and Southwest Guizhou, which has a large population of ethnic minorities, is the center of genetic diversity of rice landraces in the province; this region had the highest He at 0.7823 and the highest polymorphic information content (PIC) at 0.7562. (2) A neighbor-joining (NJ) phylogenetic tree and a model of the population structure showed that the rice landraces from the southwest, south, and southeast of Guizhou had unique genetic structures and genetic backgrounds, which are closely related to the traditional diet cultures of the local ethnic minorities. (3) A nucleotide variation analysis of similar rice landraces collected in 1980 and 2015 revealed that, after 35 years of domestication by ethnic minorities, the original dominant haplotypes were well-preserved; the frequency of the most favorable haplotypes gradually increased to adapt to the traditional food culture. This study is expected to promote the protection and sustainable utilization of rice landraces from this unique region and to provide valuable germplasm materials and information for future rice breeding and basic research efforts.

1. Introduction

Guizhou Province, located in Southwest China, has a complex terrain and a diverse climate. The unique natural environmental conditions have resulted in rich rice germplasm resources, and this region harbors an important segment of the genetic diversity of rice germplasm resources in China and worldwide [1]. Guizhou Province also has a large population of ethnic minorities. The specific traditional food cultures of these ethnic minorities have led to unique breeding and domestication methods of rice germplasm resources, creating many rice landraces with superior qualities [2]. Some rice landraces have obvious and unique regional characteristics, and these are often accompanied by a natural tolerance to stressors such as drought, cold, disease, and insect feeding; thus, these germplasms have attracted extensive attention from rice breeders and other scientists [3,4]. As a part of crop genetic resources, rice germplasm resources are an important part of the biodiversity and also an essential strategic resource of a country [5]. With the deterioration of the worldwide natural environment, some important genetic resources are rapidly declining, and the conservation and sustainable use of genetic resources have become of global concern [6]. Rice genetic diversity is the basis of variety improvements and is essential for its production; however, the breeding and improvement of rice resistance to diseases, insects, and stress tolerance has been slow in the world; one of the main reasons is the narrow genetic base of the parents used in breeding [7]. In addition, with the expansion of hybrid varieties, the planting scales of rice landraces have decreased gradually, resulting in variety simplifications, accompanied by the loss of numerous genes and reduced crop genetic diversity [8]. Thus, studies on the genetic diversity of rice are of great significance to the healthy development of the seed industry. Molecular markers are reliable genetic markers, which are rich in variation, stable in heredity, and high in polymorphisms, so the technology of microsatellite marking was broadly applied in crop genetic marking research recently [9].
The traditional food cultures of ethnic minorities can have profound impacts on local crop varieties, a phenomenon that has been addressed by many studies both domestically and internationally. Some scholars have found that the preservation and maintenance of diversity in local crop varieties in Europe are closely related to the local traditional food cultures [10]. Asian rice farmers continue to plant thousands of varieties of rice with different taste qualities to satisfy consumers with a variety of traditional food cultures [11]. Influenced by the traditional Chinese preference for glutinous rice, people living in East and Southeast Asia generally prefer waxy foods that are made from glutinous rice; in the cultivation and domestication of crops, many glutinous varieties have been bred consciously, resulting in a rich diversity of waxy germplasm resources [12]. In China, research into the influences of traditional ethnic minority food cultures on crops began relatively recently and has mainly been concentrated in Southwest China. Some investigations into genetic resources in crops in the Yunnan Province have found that many rice and wheat varieties have been lost, leaving only a few precious crop varieties cultivated in ethnic minority villages [13,14]. Furthermore, the genetic diversity of crop varieties planted by different ethnic minorities varied greatly due to differences in traditional food culture [15,16].
Guizhou Province has rich rice germplasm resources [17], primarily consisting of landraces [18]. Rice landraces are rich and diverse, particularly in areas inhabited by ethnic minorities. Previous studies have shown that the traditional dietary cultures of ethnic minorities have protected these local rice landraces [19]. A large number of ethnic minorities subsist on rice in Guizhou Province, primarily in the south, southwest and southeast. Many Miao people living in the south of Guizhou have a custom of eating colored rice, so they have bred and preserved numerous precious red rice landraces; these are primarily distributed in high-altitude mountainous areas and therefore have strong cold resistance and alpine adaptability [20]. The Buyi people in Southwest Guizhou tend to eat upland rice; Southwest Guizhou is therefore the differentiation center of upland rice genetic diversity in China [21]. The Dong people in Southeast Guizhou consume glutinous rice as a staple food at every meal [22]. There is also a world-famous “glutinous rice culture” in the southeast of Guizhou, and local ethnic minorities have bred many glutinous rice landraces [23,24]. Over the years, scholars have performed a great deal of research on rice landraces in Guizhou Province, collecting samples [18,19], measuring phenotypes [1,25], and evaluating the genetic diversity [3]. However, the overall utilization of rice resources in Guizhou Province is low, especially those rice landraces planted in the living areas of ethnic minorities. There is a lack of horizontal comparative research of rice landraces throughout the whole province and of landraces within a single region across different time periods. Therefore, the effects of ethnic minorities’ traditional dietary cultures on the genetic diversity and population structure of rice landraces are still unclear.
Here, 598 rice landraces distributed across six ecologically distinct rice farming zones in Guizhou were selected. We explored the genetic diversity of the rice landraces in this region using Simple Sequence Repeat (SSR) markers to reveal the high genetic diversity and unique population structure of rice landraces distributed in minority areas. In addition, using rice landraces from minority-inhabited areas in Southeast Guizhou Province as a case study, we studied a set of rice landraces collected in 1980 and 2015. SSR markers and single-nucleotide polymorphism (SNP) haplotype sequencing were used to explore the influence of traditional ethnic minority dietary cultures on the genetic diversity of rice landraces. This study is expected to promote the protection and sustainable utilization of rice landraces and to provide valuable germplasm materials and scientific support for rice breeding and basic research.

2. Materials and Methods

2.1. Plant Materials

Two types of rice accessions were used in this study. First, we used 640 accessions stored in the National Gene Bank, which were collected in 1980 (Table 1 and Figure 1). This collection included 598 rice landraces (Oryza sativa) from across 72 counties within six ecologically distinct rice farming zones in Guizhou Province (P1–P6) and 42 wild rice (Oryza rufipogon) accessions. An average of five accessions were selected from each county; due to the diversity of rice landraces in areas primarily inhabited by ethnic minorities, eight to nine accessions were selected from those counties. We divided P4 into two parts due to P4 being a region inhabited by large population of ethnic minorities; they have rich and diverse rice landraces, and the number of accessions used from this region is much more than other regions. In addition, the region of P4 belongs to two different ethnic autonomous prefectures inhabited by different ethnic minorities, and they have different traditional food cultures and cultivate various rice landraces with different genetic backgrounds.
The second set of accessions used in this study comprised 164 rice landraces collected by our team in Southeast Guizhou in 2015. These accessions were collected from the same parts of region P4-2 as those from the National Gene Bank collection and had the same genetic backgrounds; they were used as control accessions for the short-term domestication of ethnic minorities. The names of all the accessions used in this study are shown in Supplementary Tables S1 and S2.

2.2. DNA Extraction and SSR Molecular Marker Assays

All research accessions were planted in Hainan Province, China. The total genomic DNA was extracted manually from fresh young leaves using a modified CTAB procedure [26]. The DNA concentration was determined using a Nano Drop 2000 spectrophotometer (Thermo Fisher Scientific, Waltham, MA, USA), and the DNA integrity was checked by electrophoresis on 1% agarose gels. According to the results of previous studies [7,27], 36 SSRs (Supplementary Table S3) with good amplification and high polymorphism were used for genotypic identification, which distributed throughout the rice genome evenly. PCR amplifications were carried out using the following thermal cycling program: a pre-denaturation step at 94 °C for 5 min, followed by 35 cycles of 94 °C for 30 s, 50–60 °C for 30 s, and 72 °C for 1 min, with a final extension at 72 °C for 5 min. The PCR products were sequenced by TSINGKE on a 3730XL DNA sequencer (Applied Biosystems Inc, Waltham, MA, USA). The fragment lengths were analyzed using Gene Marker v1.6 (Soft Gene, State College, PA, USA), and the data were retained for later analysis.

2.3. Population Structure and Differentiation and Haplotype Analysis

We estimated the genetic diversity and population structures of 640 accessions with software Power Marker v3.25 [28] and STRUCTURE v2.3.4 [29,30], respectively. Nine standalone runs were designed for each k value (from 2 to 10) with the following parameters: burn-in length, 100,000 and run length, 100,000. A neighbor-joining (NJ) cluster analysis was carried out using Mega 11 and Power Marker v3.25.
According to the information provided by local people, combined with the existing research [22], rice landraces from Southeastern Guizhou are more resistant to cold, bacterial blight, and brown planthopper. Six unlinked nuclear loci across the rice chromosomes (SKC1, SAP8, Pid3, Xa23, GS5, and Ehd1) among the reported cloned genes [31,32] were used in this study to compare the nucleotide variations and haplotypes of rice landraces from Southeastern Guizhou collected in 1980 and 2015 (Supplementary Table S4). For the detection of genes, PCR amplification was carried out using the following thermal cycling program: pre-denaturation at 94 °C for 5 min, followed by 35 cycles of 94 °C for 30 s, 55–62 °C for 30 s, and 72 °C for 1 min, with a final extension at 72 °C for 10 min. Sequencing reactions were performed using an ABI 3730 automated sequencer (Applied Biosystems, USA). Initially, all samples were directly sequenced. ClustalX1.83 [33] was then used to remove redundant fragments at either end, align the sequences, and filter erroneously aligned nucleotides. We then used the Multi-Domain Analysis in DnaSP v5.0 [34], using Network4.5 [35] to construct the haplotype network.

3. Results

3.1. Statistical Analysis of Total Genetic Diversity

Using 36 selected SSR markers, we performed fluorescence-labeled SSR genotyping using capillary electrophoresis on the 598 rice landraces from Guizhou Province and on 42 wild rice accessions as a contrast (Table 2). A total of 846 alleles were detected, with the number of alleles for each marker varying from 6 (RM495) to 55 (RM206), with an average of 23.5. Alleles of RM206, RM592, RM228, and RM257 were particularly abundant, with 55, 48, 42, and 42, respectively. The genetic diversity index (He) of the 36 pairs of SSR loci varied from 0.5257 (RM495) to 0.9503 (RM206), with an average of 0.7824. The heterozygosity (Ho) ranged from 0.0578 (RM180) to 0.3875 (RM257), with an average of 0.1648, and the polymorphic information content (PIC) ranged from 0.4274 (RM495) to 0.9482 (RM206), with an average value of 0.7586, indicating that 36 SSRs had high polymorphisms. These different indices showed that the SSRs had many differences between rice accessions, indicating a high genetic diversity; the 36 SSRs used in this study could be effectively applied to the analysis of the genetic diversity of rice landraces.
Wild rice had the highest He, Ho, and PIC values (0.8526, 0.5833, and 0.8374, respectively) (Table 3), indicating that wild rice had abundant genetic variations due to long-term natural propagation and growth. For the rice landraces from Guizhou Province, the major allele frequency (MAF) varied from 0.3095 (P6) to 0.4864 (P2), with an average of 0.3519. The average number of alleles (alleles/locus, A) varied from 9.2500 (P6) to 14.9167 (P1), with an average of 23.5230. The values of MAF and A showed the low genetic diversity of P6. In additional, the differences between the above data indicate differences in the genetic diversities among populations from different regions. The P4-1 population had the highest genetic diversity (He = 0.7823), indicating that the rice genetic diversity was highest in the southwest. The genetic diversity was also high in P3 (He = 0.7549) and in P4-2 (He = 0.7334). Notably, the PIC values of P4-1, P3, and P4-2 are among the top three (0.7562, 0.7278, and 0.7233, respectively), all of which are higher than the average level (0.7501). P3, P4-1, and P4-2 are the areas of Guizhou Province where ethnic minorities subsist primarily on rice. This indicates that ethnic minorities have abundant genetic variations in rice landraces, which may be a result of their traditional food cultures. It is worth noting that P4-2 has the lowest heterozygosity (Ho), indicating that the rice landraces from Southeastern Guizhou were domesticated by the ethnic minorities for a long time with similar genetic backgrounds and a high homozygous rate.

3.2. Population Genetic Analysis with SSR Markers

To assess the population structures of rice landraces in different ecologically distinct rice farming zones of Guizhou, we constructed a neighbor-joining (NJ) phylogenetic tree using SSR data for the 640 accessions (Figure 2). The NJ tree was divided into three groups: Group I (wild rice), Group II (japonica landraces), and Group III (indica landraces). For indica accessions, the population structure was not directly related to the geographical origin of the landraces; all accessions were mixed within each cluster, indicating that the genetic backgrounds of indica rice landraces in Guizhou are relatively complex. However, japonica was clearly divided into three subgroups. Subgroup 1 contained the P4-2 population from Southeastern Guizhou. The landraces in this subgroup have long been cultivated and domesticated by the local Dong people. Subgroup 2 contained the P3 and P4-1 populations from Southwestern Guizhou. These landraces have long been cultivated and domesticated by the local Buyi and Miao people. Subgroup 3 contained the P1, P2, P5, and P6 populations and the accessions from all of these regions clustered together. The minority populations are relatively small in these areas.
To further study the population structure of the 640 rice landraces, a Bayesian analysis was performed using STRUCTURE v2.3.4 [30]. Following a method proposed by Evanno et al. [36] to detect natural population clustering, we determined the number of subgroups within each population. There were two distinct peaks in the ΔK graph at K = 2 and K = 8 (Figure 3), supporting the division of the population into two or eight subgroups. When K = 2, the population was divided into two subgroups: japonica and indica; at K = 8, the results were consistent with those of the NJ tree. The Indica accessions were not further separated by region, whereas the japonica landraces from P3, P4-1, and P4-2 were clearly distinguished, and other accessions were clustered together with those from other regions (Figure 4). The results from NJ clustering and the STRUCTURE analysis indicated that the population structure was significantly different for japonica landraces from P3, P4-1, and P4-2 compared to other regions. The analysis suggested that this was related to the traditional food cultures of the ethnic minorities living in these regions.

3.3. Genetic Variation in Rice Landraces before and after Short-Term Domestication by Ethnic Minorities

To further study the short-term domestication of rice landraces resulting from the influence of traditional ethnic minority food cultures, we compared the dynamic changes in the genetic diversity of two populations collected in 1980 (142 accessions) and 2015 (164 accessions). Both populations were collected from Southeastern Guizhou, and most accessions bore the same local name at both time points. Thirty-six SSR markers were used to detect the genetic diversity of these rice landraces from Southeastern Guizhou. A total of 561 alleles were detected, with the number of alleles for each marker varying from 6 (RM135 and RM495) to 39 (RM592), with an average of 15.6. Alleles of RM592, RM206, RM219, RM257, RM247, and RM333 were particularly abundant, with 39, 37, 36, 30, 27, and 23, respectively. The results of the genetic diversity analysis showed that the main allele frequency (MAF), He, and PIC were higher in the rice landraces collected in 2015 than in 1980 (Figure 5). This indicated that traditional domestication by ethnic minorities has increased the genetic diversities of rice landraces and that in situ conservation by farmers has a positive role in promoting genetic diversities. An analysis of molecular variance (AMOVA) showed that 3.43% of the genetic variations could be attributed to differences between the populations collected at different time points, whereas 89.35% of the genetic variations were within-sample variations. Therefore, the genetic variations mainly come from within each population.
Compared with those from other regions, rice landraces from Southeastern Guizhou have large grain sizes, short growth stages, high cold and salt tolerances, and high resistance against insects and diseases [37,38,39]. Six related, nonlinked nuclear gene loci (SKC1, GS5, Pid3, SAP8, Ehd1, and Xa23) were sequenced. The sequence length of each locus was 3700 bp, with a range of 482–670 bp. DnaSP v5.0 was used to estimate the haplotypes and genetic diversity at different loci in the accessions collected in 1980 and 2015 (Table 4). The number of polymorphic sites (S) in the six genes varied between the 1980 and 2015 populations, showing different nucleotide polymorphisms. The nucleotide diversity (π) values of the landraces ranged from 0.00071 (SAP8) to 0.00472 (Pid3), with an average value of 0.00299 in the 1980 population; in the 2015 population, the π values ranged from 0.00017 (SAP8) to 0.00491 (Pid3), with an average value of 0.00327, representing a significant difference from the 1980 population (p < 0.05). θw values indicated polymorphisms of segregating sites. For each gene, the rice landraces had significantly different θw values in 2015 than in 1980 (an average of 0.00248 vs. 0.00204, respectively; p < 0.05). The π and θw values indicated that there were more polymorphisms in the 2015 rice landrace populations than in the 1980 populations. This suggested that traditional domestication by ethnic minorities had a positive effect on rice landrace diversity.
The neutrality measures were calculated for each locus, namely Tajima’s D value, Fu and Li’s D* value, and Fu and Li’s F* value (Table 4). Tajima’s D values were significant for four genes in the 2015 population; the positive D values for Pid3 (2.43142) and Xa23 (1.64574) indicated that there were many moderate-frequency polymorphisms in these two loci. These were the result of balanced selection in the domestication process for rice blast resistance and bacterial blight resistance. The negative D values of GS5 (−1.89378) and Ehd1 (−2.26868) indicated that there were a large number of low-frequency polymorphisms in the genes related to rice grain size and the heading stage regulation after 35 years of domestication by ethnic minorities. These low-frequency polymorphisms were rare allelic loci that were subjected to either negative or strong positive selection. Four-gamete testing revealed that the minimum number of recombination events (Rm) ranged from 0 to 3 in landraces from 1980 and in those from 2015; the average values for those from 1980 and from 2015 were 1.2 and 1.5, respectively. There was no significant difference in Rm between the two populations from different time periods, indicating that the degree of heterozygosity was similar between the two populations.

3.4. Network Relationships of Haplotypes Based on Target Genes

The haplotype numbers of rice landraces from 1980 and 2015 were 6, 4; 7, 5; 8, 5; 4, 2; 4, 4 and 9, 7 at the SKC1, GS5, Pid3, SAP8, Ehd1, and Xa23 gene loci, respectively (Figure 6). A total of 73.0% of the haplotypes were retained in the rice landraces from 2015, and most were dominant haplotypes. Moreover, four rare haplotypes (Hap5 of Ehd1, Hap8 and Hap10 of Pid3, and Hap8 of GS5) were newly developed, suggesting the original dominant haplotypes were well-maintained after short-term selective domestication by minorities.
The frequency of the dominant haplotypes also changed between the 1980 and 2015 populations (Figure 7). For most of the dominant haplotypes, such as Hap1 of SKC1, GS5, SAP8, and Ehd1, the frequency increased to >95% in the 2015 population. In addition, Hap3 of SKC1, Pid3, and Xa23 were common haplotypes in the 1980 population (frequency > 15%) but were rare in the 2015 population (frequency < 5%). This result indicates that the haplotypes of these genes may have been selected by natural and artificial selection as the result of traditional domestication by ethnic minorities. The frequency of most favorable haplotypes for agronomic traits and stress resistance gradually increased, whereas the frequency of some unfavorable haplotypes gradually decreased.
The circle size is proportional to the quantity of samples within a given haplotype, and the numbers next to the circle represent the haplotype type. Lines between different haplotypes represent the mutational steps between alleles. When more than one nucleotide difference existed between two linked haplotypes, the number of differences is shown next to the line. Yellow represents landraces collected in 1980, and pink represents landraces collected in 2015.

4. Discussion

4.1. Evaluation of Genetic Diversity in Rice Landraces

Genetic diversity is an important basis for rice breeding, genetic improvement, and rice production [7]. Southwest China is considered to be one of the origins and diversity centers of cultivated rice in Asia [40], and many scholars have therefore studied the genetic diversity of rice landraces in this area using SSR markers. Yang et al. analyzed the genetic diversity of 63 rice landraces in Yunnan and showed that the He was 0.7187 [41]. Chen et al. studied more rice landraces in Yunnan (908) and calculated the He as 0.7307 [42]. Studies of rice populations using fewer or more accessions have confirmed the high genetic diversity of rice landraces in Yunnan. Guizhou Province, which borders Yunnan Province and also has rich rice landrace resources.
In this study, a total of 846 alleles were detected using 36 pairs of SSR markers covering 12 chromosome pairs in rice. The number of alleles per marker ranged from 6 to 55, with an average of 23.5 alleles per marker, which was higher than previous studies, including 40 rice landraces in Yunnan Province with 4.46 alleles per marker [43], 50 rice varieties in India with 12.47 alleles per marker [44], and 314 rice varieties in Laos with 3.49 alleles per marker [45]. In additional, the He of 598 landraces in Guizhou was 0.7721, which was higher than previously calculated for this region; a set of 537 indica and japonica rice varieties in Guizhou was previously reported to have an He value of 0.6960 [40], and 147 red rice varieties in Guizhou were calculated to have an He value of 0.3549 [20]. This finding indicated that the genetic diversity of rice landraces was high and that the genetic background was rich in six ecologically distinct rice farming zones in Guizhou. This is related to the complex and changeable climatic conditions, rich and diverse ecological environments, and unique traditional food cultures of Guizhou Province. The diversity of rice landraces in Guizhou Province is of great significance in breeding new rice varieties and broadening the genetic basis of cultivated rice.
Meanwhile, the P4-1 region in Southwestern and Southern Guizhou had an average of 115,000 alleles per locus, and this population had the highest He (0.7823) and PIC (0.7562). These results were consistent with the results of Zhang et al. [40], indicating that this is the center of the rice landrace genetic diversity in the province. Future intensive research using rice landraces from this region will allow for the more effective use of these excellent rice resources to explore novel genes and breed new varieties.

4.2. Synergistic Evolution of Rice Landraces and Traditional Dietary Cultures

Rice landraces are no longer cultivated in most provinces in China, with the exception of some ethnic minority regions in areas such as Guizhou Province (RCUIDI). The diversity and population structures of rice landraces are affected by many factors, not only including environmental and genetic factors but also traditional farming activities and food cultures [46]. The traditional dietary cultures of ethnic minorities often include traditional wisdom related to crop production and emphasize the holistic nature of the relationship between the community and the land [47]. We therefore believed that rice landraces have evolved in coordination with the traditional dietary culture and farming activities of ethnic minorities. Traditional genetic resources played a key role in the generation and development of ethnic traditional dietary cultures. Ethnic traditional dietary cultures also promoted the protection and sustainable utilization of genetic diversity. Therefore, the preservation of genetic resources and the protection of ethnic traditional cultures were interdependent and mutually reinforcing relationships. Relevant studies showed the positive influence of ethnic minorities on genetic diversity. For example, some scholars believe that, in some Southeast Asian countries, such as Vietnam and Nepal, the rich and diverse dietary cultures of the local ethnic minorities have promoted the conservation of rice genetic diversity [48,49]. According to Wang et al. [27], the rich genetic resources of rice landraces in Southwest China are due to the numerous traditional festivals and rich diet cultures of the local ethnic minorities. Southwestern Guizhou (Qianxi’nan), Southern Guizhou (Qiannan), and Southeastern Guizhou (Qiandongnan) are all special ethnic autonomous prefectures in Guizhou Province. Autonomous prefectures are a type of administrative division in China that have the same administrative status as prefecture-level cities and are the primary areas inhabited by ethnic minorities. The number of ethnic minority villages and the populations of the ethnic minorities in these three regions are high, and they have unique food cultures [50,51]. We therefore conclude that the traditional dietary cultures of ethnic minorities in these regions have led to the domestication of local rice landraces into special ecological types with unique genetic backgrounds.
In modern Asian cultivated rice, the primary genetic differentiation is between indica and japonica varieties; intraspecific structure or classification within indica and japonica has been the focus of a great deal of research [52]. We here found that the indica varieties in Guizhou Province did not cluster together based on geographical origin, indicating that the genetic basis of indica was broad and may have had different sources. This was consistent with the research by Xian et al. [53], which showed that indica has historically been introduced several times in Guizhou, gradually replacing local glutinous rice to increase the grain yields and meet the basic needs of the local people [54]. In contrast, the population structure of japonica in Guizhou was correlated with the geographical origin; this was especially true of landraces from regions P3, P4-1, and P4-2, members of which formed individual clusters. This indicates that rice landraces may form unique genetic backgrounds as a result of the influence of traditional dietary cultures. Due to domestication and artificial selection, these rice landraces often have outstanding resistance to diseases, insects, and other stressors, making them ideal materials for breeding and highlighting the need to strengthen the protections for and increase the research efforts using these unique resources [55].

4.3. Effective Conservation Mechanisms of Genetic Diversity in Rice Landraces

Conservation methods for rice landraces include in situ (i.e., on-farm) and ex situ (i.e., gene bank) approaches, which each have advantages and disadvantages. At present, many countries place a great deal of emphasis on the construction of crop gene banks to enable the protection of as many genetic resources as possible [56,57]. However, in situ conservation can not only maintain the continuous evolution of landraces in their original habitat but also includes the protection and utilization of landrace resources through the participation of and selection by farmers; traditional cultural customs and farming methods can effectively increase their genetic backgrounds and genetic diversities [7,58]. The results of this study confirmed that continuous selection and domestication by ethnic minorities effectively improved the genetic diversity of rice landraces.
Ethnic minorities living in Southeastern Guizhou have well-maintained the original dominant haplotypes of rice landraces, and the frequency of most favorable haplotypes has increased. This effect may be related to the traditional food cultures of ethnic minorities, who serve as cultivators of rice landraces and consistently protect many ancient local varieties [59]. Therefore, the protection of traditional ethnic minority food cultures inherently protects the diversity of local rice landraces. Ex situ conservation is also an important method that preserves the genetic integrity and diversity of crops without risking disappearances or changes over time [60].

5. Conclusions

The results of this study revealed high genetic diversities and rich genetic backgrounds in the rice landraces collected from six ecologically distinct rice farming zones in Guizhou Province. The genetic diversity was especially high and the population structures unique in landraces from the southwest, south, and southeast regions; these regions contain large populations of ethnic minorities, who have traditional dietary cultures related to unique rice characteristics. The southwest of Guizhou is the center of genetic diversity in rice landraces in China, and it is therefore necessary to strengthen the utilization and protection of the local rice resources. The nucleotide variation analysis of a similar set of rice landraces collected in 1980 and in 2015 showed that the genetic diversity increased over the intervening 35 years, and the original dominant haplotypes of the rice population were preserved. Moreover, the frequencies of the most favorable haplotypes gradually increased, whereas the frequencies of a few unfavorable haplotypes gradually decreased through adaptation to the corresponding traditional food cultures. This study provides valuable new insights for future rice breeding and basic research efforts and is expected to promote the protection and sustainable utilization of rice landraces.

Supplementary Materials

The following supporting information can be downloaded at https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/agronomy12102308/s1: Table S1: Six hundred and forty accessions collected in 1980. Table S2: One hundred and sixty-four accessions collected in 2015. Table S3: SSR primer information. Table S4: Summary of the gene sequences and the primer sequences used in this study.

Author Contributions

C.L. and Y.W. were the principal researchers who conducted the field research, Y.W. conceived and designed the experiments, C.L. analyzed the data analysis and drafted the manuscript, and D.X. and L.H. were supervisors who initiated and provided oversight to the study and input during its planning and provided ethic and cultural advice based on their rich experience and knowledge. A.J., X.M., D.C., X.L., B.H., H.C. and R.R. carefully revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China (2021YFD1200500); the National Natural Science Foundation of China (31901487); CAAS Science and Technology Innovation Program, National Crop Germplasm Resources Center (NCGRC-2021-2); The Program of Protection of Crop Germplasm Resources (19200385-1); The Third National General Survey and Collection Action of Crop Germplasm Resource (19210859 and 19210860); and the biodiversity investigation, observation, and assessment program (2019-2023) of the Ministry of Ecology and Environment of China; the National Natural Science Foundation of China (32171669).

Data Availability Statement

All data supporting the findings of this study are available within the manuscript and within its supplementary materials.

Conflicts of Interest

All the authors declare that there are no conflicts of interest to disclose.

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Agronomy 12 02308 g001 550
Figure 1. The six ecologically distinct rice farming regions in Guizhou Province.
Figure 1. The six ecologically distinct rice farming regions in Guizhou Province.
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Figure 2. Neighbor-joining cluster analysis of 640 rice accessions based on SSR markers.
Figure 2. Neighbor-joining cluster analysis of 640 rice accessions based on SSR markers.
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Figure 3. The statistic ΔK value for each given K in the population structure analysis.
Figure 3. The statistic ΔK value for each given K in the population structure analysis.
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Figure 4. Model-based ancestries and their distribution in the indica, japonica, and wild rice groups.
Figure 4. Model-based ancestries and their distribution in the indica, japonica, and wild rice groups.
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Figure 5. Comparison of the genetic diversities between populations collected in 1980 and 2015. MAF, major allele frequency; He, gene diversity; Ho, heterozygosity; and PIC, polymorphic information content.
Figure 5. Comparison of the genetic diversities between populations collected in 1980 and 2015. MAF, major allele frequency; He, gene diversity; Ho, heterozygosity; and PIC, polymorphic information content.
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Figure 6. Haplotype networks for six loci in the rice accessions collected in 1980 and 2015.
Figure 6. Haplotype networks for six loci in the rice accessions collected in 1980 and 2015.
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Figure 7. Changes in the haplotype frequency in a set of rice accessions collected in 1980 and 2015.
Figure 7. Changes in the haplotype frequency in a set of rice accessions collected in 1980 and 2015.
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Table
Table 1. Basic information of rice landrace accessions used in this study.
Table 1. Basic information of rice landrace accessions used in this study.
Types of AccessionsCategoryPopulationGeographic DistributionNumber of AccessionsRelease Time
The first set of accessionsRice landracesP1Central Guizhou1901980
P2Eastern Guizhou451980
P3Southwestern Guizhou851980
P4-1Southwestern and southern Guizhou841980
P4-2Southeastern Guizhou1421980
P5Northern Guizhou231980
P6Northwestern Guizhou291980
Wild rice (WR)P7Guangdong, Guangxi, and
Hunan provinces		421980
The second set of accessionsRice landraces/Southeastern Guizhou1642015
Table
Table 2. Summary of genetic diversity among 640 accessions at 36 SSR loci.
Table 2. Summary of genetic diversity among 640 accessions at 36 SSR loci.
MarkerChrNaHeHoPICMarkerChrNaHeHoPIC
RM448190.85580.07340.8411RM22810420.86830.23750.8571
RM28711130.80070.12190.7764RM2111220.67860.15160.6579
RM3367210.84910.16410.8351RM4491240.80750.14530.7840
RM1353110.60100.09690.5213RM23512210.78320.11880.7668
RM2495250.59390.11090.5446RM24712350.85270.15780.8435
RM187260.84560.17340.8278RM1712170.67420.12340.6284
RM1807160.53990.05780.5141RM2536190.87120.10310.8587
RM2513250.79170.10630.7785RM3354250.85960.10940.8484
RM4305320.80390.11410.7887RM2238200.82610.1250.8083
RM20611550.95030.28440.9482RM2804240.64990.11880.6224
RM5925480.93870.08910.9359RM25810130.57710.10940.5357
RM2766270.86810.10310.8557RM2414270.88440.15160.8753
RM2082120.57790.26560.5519RM33310280.92980.32970.9253
RM2132160.77780.28910.7456RM5846160.74380.13590.7006
RM2199390.90930.30630.9027RM5252150.81620.27810.7972
RM2201250.85090.19840.8351RM68388110.72790.09530.6850
RM495160.52570.06720.4274RM2859100.79350.30310.7658
RM2312190.82970.12970.8092RM2579420.91370.38750.9097
Chr, chromosome; Na, observed number of alleles; He, genetic diversity; Ho, heterozygosity; and PIC, polymorphic information content.
Table
Table 3. Summary statistics for the genetic diversity of 640 rice accessions.
Table 3. Summary statistics for the genetic diversity of 640 rice accessions.
PopulationNMAFAHeHoPIC
P11900.392114.91670.70160.13450.7107
P2450.48649.55560.65780.15620.6283
P3850.371712.86110.75490.13590.7278
P4-1840.464611.50000.78230.15580.7562
P4-21420.383613.16670.73340.10470.7233
P5230.37687.72220.71960.13890.7015
P6290.30959.25000.70500.19640.6959
P1–P65980.351923.52300.77210.16480.7501
Wild rice420.241415.69440.85260.58330.8374
N, sample size; MAF, major allele frequency; A, alleles/locus; He, genetic diversity; and Ho, heterozygosity.
Table
Table 4. Summary of nucleotide polymorphisms and neutrality test.
Table 4. Summary of nucleotide polymorphisms and neutrality test.
GroupGeneShHdπθwDD*F*Rm
1980SKC1560.5360.001710.001470.33442−0.105790.04880
GS51270.5110.004640.003490.83449−1.22227−0.562912
Pid31080.690.004720.00271.80688−0.142170.661693
SAP8340.4610.000710.00080.00080.00080.00080
Ehd1540.4870.003920.001862.21023 **1.004851.6661
Xa23790.7640.002230.001940.333330.245080.327231
Average76 **0.5750.002990.002040.92003−0.036580.356941.2
2015SKC1540.5590.002170.00115−1.54948−1.64515 *−1.90910
GS51250.5810.004810.00448−1.89378 **−1.96452−2.31825 *3
Pid31150.6340.004910.002852.43142 **1.153861.89957 *3
SAP8320.5470.000170.00096−0.763870.463030.100171
Ehd1540.6810.004650.00282−2.26868 **−0.13207−0.609251
Xa23870.7610.002930.002621.64574 **0.060340.309131
Average75 **0.627 **0.00327 *0.00248 *−0.39978−0.34409−0.421291.5
S, number of polymorphic (segregating) sites; h, number of haplotypes; Hd, haplotype (gene) diversity; π, nucleotide diversity; θw, Watterson’s parameter for silent sites; D, Tajima’s D; D*, Fu and Li’s D* value; F*, Fu and Li’s F* value; and Rm, minimum number of recombination events. * p < 0.05 and ** p < 0.01.
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Liu, C.; Wang, Y.; Jiao, A.; Ma, X.; Cui, D.; Li, X.; Han, B.; Chen, H.; Ruan, R.; Xue, D.; et al. Effects of Traditional Ethnic Minority Food Culture on Genetic Diversity in Rice Landraces in Guizhou Province, China. Agronomy 2022, 12, 2308. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12102308

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Liu C, Wang Y, Jiao A, Ma X, Cui D, Li X, Han B, Chen H, Ruan R, Xue D, et al. Effects of Traditional Ethnic Minority Food Culture on Genetic Diversity in Rice Landraces in Guizhou Province, China. Agronomy. 2022; 12(10):2308. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12102308

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Liu, Chunhui, Yanjie Wang, Aixia Jiao, Xiaoding Ma, Di Cui, Xiaobing Li, Bing Han, Huicha Chen, Renchao Ruan, Dayuan Xue, and et al. 2022. "Effects of Traditional Ethnic Minority Food Culture on Genetic Diversity in Rice Landraces in Guizhou Province, China" Agronomy 12, no. 10: 2308. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12102308

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