African Journal of
Biotechnology

  • Abbreviation: Afr. J. Biotechnol.
  • Language: English
  • ISSN: 1684-5315
  • DOI: 10.5897/AJB
  • Start Year: 2002
  • Published Articles: 12487

Full Length Research Paper

Genetic diversity of Faidherbia albida populations in the Sudano Sahelian region of Cameroon, using simple sequence repeat (SSR) markers

T. Dorothy Tchatchoua
  • T. Dorothy Tchatchoua
  • Department of Ecosystem Science and Management, Pennsylvania State University, University Park PA 16802 USA.
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R. Scott Poethig
  • R. Scott Poethig
  • Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USA.
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Erin Doody
  • Erin Doody
  • Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USA.
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T. Casey Weathers
  • T. Casey Weathers
  • Department of Ecosystem Science and Management, Pennsylvania State University, University Park PA 16802 USA.
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Krystle Swartz
  • Krystle Swartz
  • Department of Ecosystem Science and Management, Pennsylvania State University, University Park PA 16802 USA.
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Iain Mathieson
  • Iain Mathieson
  • Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia. PA 19104, USA.
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Nicole Zembower
  • Nicole Zembower
  • Department of Ecosystem Science and Management, Pennsylvania State University, University Park PA 16802 USA.
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Tetyana Zhebentyayeva
  • Tetyana Zhebentyayeva
  • Department of Ecosystem Science and Management, Pennsylvania State University, University Park PA 16802 USA.
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John E. Carlson
  • John E. Carlson
  • Department of Ecosystem Science and Management, Pennsylvania State University, University Park PA 16802 USA.
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  •  Received: 06 May 2020
  •  Accepted: 06 July 2020
  •  Published: 31 July 2020

 ABSTRACT

Faidherbia albida (DEL.) A. Chev is widely grown in the northern region of Cameroon because of its many benefits to local communities. However, droughts and deforestation have led to decreases in the abundance of this species, increasing the need to identify improved genotypes for conservation, management, and breeding. The genetic diversity of F. albida in nine populations from the Sudano-Sahelian region of northern Cameroon was characterized using microsatellite (SSRs) markers. A total of 28 alleles were recorded across 8 loci and 255 samples. The effective mean number of alleles per locus was 2.3. Observed heterozygosity ranged from 0.24 to 0.30, while expected heterozygosities ranged from 0.22 to 0.26. For most loci, FIS was negative. Higher variation was observed within than among the northern Cameroon populations, and principal component and admixture analyses did not reveal any population substructure. Phenotypic diversity in 3-month-old seedlings was also characterized and significant within population variation was found for most morphological traits. Although some populations differed significantly for one or more traits, in general the populations were phenotypically similar. These results suggest little barrier to gene flow between populations of F. albida in northern Cameroon, and that no single provenance is likely to be superior for selection and breeding purposes.

 

Key words: Faidherbia albida, phenotypic, genotypic, variation, populations, breeding.


 INTRODUCTION

The North and Far North regions of Cameroon are located in the Sahel, and are characterized by Sudano-Sahelian vegetation. This vegetation contains a variety of forest tree species, such as Adansonia digitata (Baobab), Acacia senegal, Acacia nilotica, Faidherbia albida, Vitellaria paradoxa (Shea butter), Tamarindus indica (Tamarind) and Azadirachta indica (Neem), with great multipurpose   potential.   Collectively,    these   trees  are
 
economically important sources of timber, building poles, and non-wood products such as gums and tannins, while in some cases also improve soil fertility through nitrogen fixation and organic matter production. However, the region is susceptible to droughts, degradation and desertification which has threatened, as well as caused loss of, species and genetic diversity. Additionally, reduction in land area available for cultivation due to population explosion and growing demand for forest products have resulted in the growth of trees under marginal conditions. The importance, demand and decline of these species calls for the breeding of improved and high yielding genotypes for future planting in forests, parks and farms.
 
Faidherbia albida (Del.) A. Chev is particularly important in this region because or its unique attribute of producing leaves and fruits in the dry season, when most other trees are leafless and dormant (World Agroforestry Center, 2009). Faidherbia albida also provides shelter for animals, whose dung is used as fertilizer for food crops (Boffa, 1999; Roupsard et al., 1999). Besides providing organic fertilizer and livestock fodder, F. albida acts as windbreak, supplies wood for fuel and construction, and reduces erosion by reducing soil compaction, which facilitates water absorption during the rainy season (Peltier, 1996). For all of these reasons, F. albida was selected as a priority species for domestication (Franzel, 1996) by the World Agroforestry Center (ICRAF) and by the FAO Panel of Experts on Forest Genetic Resources (FAO, 1974). To increase soil fertility in the Far-North region of Cameroon, in 1990 the Rural Development and Management Project (DPGT) lead by SODOCOTON encouraged the planting of F. albida on farm lands and the creation of parklands through natural and artificial regeneration (Gautier et al., 2002).  Indeed, several reforestation projects in the region are currently ongoing. These projects would benefit from the availability of fast-growing genotypes resistant to biotic and abiotic stresses, but there has been little effort to identify improved genotypes of F. albida suitable for this region.
 
Forest tree genetic improvement programs typically begin with an assessment of the genetic diversity within the species of interest, to determine the amount of genetic and phenotypic variation available for selection (Muona, 1990; Wright, 1962; Franzel et al., 1996).  Seed samples are collected across the entire natural range of the species, or within a geographic area of interest, with which seedling field trials are conducted, referred to as provenance tests (Zobel and Talbert, 1984). In the case of F. albida, genetic improvement studies started three decades ago with the morphological characterization of provenances from northwest, northcentral, east and south African populations, including field trials in Burkina Faso, Zimbabwe,  Cameroon and Sudan (Sniezko and Stewart, 1989; Peltier and Eyog-Matig, 1988; Vandenbeldt, 1991, 1992; Abdelazim et al., 1997; Tchatchoua et al., 2019). These trials  revealed  two  distinct  ecotypes,  one spanning the Sahel in North Africa, and a second typically found in riparian habitats in East and South Africa. Consistent with their habitats, provenances from the Sahel have small seeds, grow relatively slowly, and are drought tolerant, whereas provenances from East and South Africa have relatively large seeds, grow quickly, and are susceptible to drought (Vandenbeldt, 1991; Dangasuk et al., 2006). Analyses of isozyme variation support this distinction, and reveal that populations from northwest and northcentral Africa are genetically more diverse than populations from east and south Africa (Harris et al., 1997; Abdelazim et al., 1997; Joly et al., 1992).
 
Microsatellite (simple sequence repeat, SSR) markers have many advantages for analyses of genetic variation because of their high reproducibility, co-dominant inheritance, multi-allelic variation and abundance in the genome (Muchugi et al., 2008; Varshney et al., 2005).  In addition, they can be evaluated relatively cheaply and at high throughput using automated platforms.  In this study, the researchers took advantage of SSRs identified in F. albida by Russell et al. (2014) to characterize the genetic diversity within 9 provenances of F. albida from the Sudano-Sahelian region of Cameroon. The primary goals of this study were to determine if these markers could be used to differentiate populations and to identify populations with sufficient genetic variation to be useful for breeding programs.


 MATERIALS AND METHODS

Germplasm collection
 
Seeds were collected indeterminately from well-spaced trees in nine populations in the distribution range of the species in the Sudano-Sahelian region of Cameroon (Table 1 and Figure 1). 50 to 100 fruit pods were collected from each of 20 trees in each population. The trees were at least 100 m apart to avoid sampling trees of the same genotype, and populations were separated by a distance of at least 100 km as proposed by Tchoundjeu et al. (1998). The seeds were extracted from the fruit by students of the National Advanced School of Engineering, University of Maroua during a practical session. Following inspection by the Plant Protection and Regulatory Services Directorate of Cameroon’s Ministry of Agriculture and Rural Development (MINADER), the seeds were sent to the Schatz Center of Molecular Genetics USA (USDA import permit OMB No. 0579 - 0049) for DNA extraction, amplification and sequencing.
 
Phenotypic analysis
 
Seeds were nicked at the micropylar end using nail clippers, being careful to avoid damaging the radicle. They were germinated for two days on moist paper towels at 30°C, and viable seeds were then planted in a mixture of 1/3 bar sand and 2/3 Scott’s Premium Topsoil in Stuewe TP38 pots. Four plants from each of 6 trees in each provenance were grown under fluorescent illumination in Conviron growth chambers on a diurnal cycle consisting of 12 h light (PAR 265 µm m-2 s-1) at 30°C, and 12 h dark at 20°C. One-half teaspoon of Osmocote slow release fertilizer was added to each pot at planting and fertilized once a month with a dilute solution of 10:20:10 fertilizer. Plants were measured 3 months after planting with the help of a stereomicroscope. Plant height was measured from the soil surface to the tip of the last leaf. The number of all leaves larger than 5 mm was recorded at the same time. Stem width was measured in the third internode, using Vernier calipers. Fully expanded leaves near the tip of the shoot were attached to paper using double sided tape, scanned into a computer, and secondary leaflet area was then measured using Image J. 
 
 
Growth of seeds and DNA extraction
 
A total of 255 seeds (that is, 3 seeds per family, 8 to 10 families per population and 9 populations) were nicked with a nail clipper and sown in polymix soil  in  4 in  plastic  pots.  Plants  were grown  in  a growth chamber (25°C, 16 h. light: 8 h dark), and leaves were harvested for DNA extraction when plants were 4 weeks old. Approximately 100 mg of leaf tissue was macerated using a TissueLyser 11 (11.5 rmp for 1 minute), and genomic DNA was then extracted using DNeasy Plant Mini Kit (Qiagen), following the manufacturer’s instructions. DNA concentrations were measured using a Qubit DNA kit (QubitTM Assays) and a working DNA concentration of 1 ng/µl solution was prepared for all samples and stored in a -80°C freezer for further use.
 
Screening of SSR primers
 
Eight DNA samples, one from each of eight families were screened with 48 SSR primer pairs previously developed for F. albida (Russel et al., 2014). PCR was performed using 1 µl genomic DNA (1 ng/µl), 2.5 µl each of 10 µM forward and reverse primers, 19 µl of Ultra-Pure water and 1 Edvo-tek bead. Samples were amplified in an Applied Biosystems thermocycler using the following conditions: 95°C for 15 mins, followed by 35 cycles of 94°C for 30 s, 55°C for 1.5 min and 72°C for 1 min, with a final extension at 72°C for 10 min. Eight primer pairs that produced clear, strong, polymorphic amplification products between 100 and 250 base pairs (bp) in length were chosen for further analyses (Table 2).
 
 
PCR amplification procedure
 
The eight selected markers were used to genotype 255 individuals from 85 families and nine populations. PCR was performed with a fluorescently labeled forward primer using the conditions described above, and the amplification products were then separated using an Applied Biosystems Illumina 3730 XL DNA sequencer at the Huck Genomic Core Facility of Pennsylvania State University, State College USA. Fragment analysis was performed with GeneMapper software at GS 500 (-200) LIZ standard size.
 
Data analysis
 
The phenotypic data were analyzed using SPSS v12 statistical package (IBM; https://www.ibm.com/products/spss-statistics) for data description and analysis of variance (ANOVA). All the measured traits assumed normal distribution and significance level for the ANOVA was at 0.05. Means comparison was conducted using the DUNCAN multiple range test (Duncan, 1955).
 
Population genetic analysis of the SSR marker results was performed within Excel using GenAlEx 6.5 (Peakall and Smouse, 2012). Summary statistics for allelic richness (the total number of alleles per locus and the effective number of alleles), unbiased observed and expected heterozygosities and the percentage of polymorphism in each population were calculated. The allelic richness (number of alleles), fixation index (FIS = inbreeding) and geneflow information were calculated with F. Stat version 2.9 3.2 (February, 2002). GenePop (https://genepop.curtin.edu.au/) was used   to   conduct   Hardy   Weinberg   Exact  tests  (HWE)  and  to estimate linkage disequilibrium at 0.05 Bonferroni corrections for pairwise comparison, genetic bottleneck, and Nei effective population size. The program ADMIXTURE v1.3.0 (Alexander et al., 2009) was used to cluster individuals into 2<K<10 clusters. The lowest cross-validation error occurred with K=2.  Analysis of molecular variance (AMOVA) (Excoffier et al., 1992) was performed as a pairwise comparison of FST (genetic fixation index) values and P-values, using GenAlEx 6.5.  Phylogenetic trees were constructed using Mega 7.027 software (Kumar et al., 1994).


 RESULTS

Phenotypic variation in F. albida populations
 
A range of morphological traits was examined to determine the degree to which populations of F. albida in Cameroon are phenotypically distinct at the seedling stage. ANOVA revealed that there was significant variation for most traits among all 9 populations (Table 3). However, no single population was consistently different from other populations (Figure 2) and, in general; the populations were morphologically quite similar (Figure 3). At three months of age, the population means for the width of the third internode ranged from 1.5 and 1.8 mm, total leaf number ranged from 29 to 39, and plants were 19 to 29 cm in height. At this stage, populations had an average of 1 to 4.5 branches greater than 1 cm in length. The most recently formed leaves had one or two pairs of primary leaflets, each with 6 or 7 pairs of secondary leaflets, which were 4 to 5 mm2 in area. Extrafloral nectaries (EFN) were typically absent from the first 4 to 10 leaves, but were present on later-formed leaves. One of the most obvious differences between populations was the frequency of glabrous (hairless) plants. Glabrous plants were either absent (Sirlawe) or a minor  fraction  of the plants in the Adoumi (11%), Dinao (22%), Kongolo (19%), Moulvoudaye (5%), and Tokombere (9%) populations, but were the major class in Mambang (87%), Mokolo (54%) and Zamai (79%) (Figures 2 and 3).
 
 
 
Genetic variation in F. albida populations
 
A set of 48 SSR markers were tested with DNAs from eight families to identify robust markers for assessing genetic variation in this study. Eight informative markers were selected as being most reproducible and informative based on agarose gel results, which were then used to genotype 255 individuals from 9 populations in Cameroon by high-resolution capillary electrophoresis. Seven of the SSR loci were polymorphic, while Locus_24 proved to be monomorphic in all of the populations studied based on GeneMapper analysis. The allele frequencies across all populations and loci are presented in Table 4 and the population genetic parameters calculated for these loci from the allele frequencies are presented in Tables 5 and 6. A total of 28 alleles were recorded across the 8 loci and 255 samples. The number of alleles observed at each locus ranged between 1 (marker 24) and 7 (marker 5), while the number of effective alleles ranged from 1 to 2.7 with a mean Ne of 1.5. The mean percentage of polymorphism was 73.6, while among populations polymorphism percentages ranged from 62 in Moulvodaye and Zamai to 87.5 in Sirlawe. Alleles 189 of Locus_22 and 195 of Locus_5 were only found in the Adoumri population. Alleles 180  and 198 of Locus_5 were only found in Moulvoudaye. Alleles 174 of Locus_30 and 153 of Locus_8 were unique to Kongola and allele 228 of Locus_11 was restricted to Dinao. As these alleles were only present at frequencies between 2 and 5%, further investigations should be conducted   to   determine   if    they   can    be    used   to
discriminate between the Cameroon populations.
 
The highest number of alleles was found in the Sirlawe, Kongola and Adoumri populations, which also had the highest Shannon diversity indices (I). The Shannon diversity index ranged from 0.000 to 1.095 among the 9 populations, with a mean of 0.417. Families DIN 10, SIR 06, and TOKO 10 showed variation in 5 loci, while families AD 26, AD 36, DIN 07, DIN 11, KON 03, KON 01, KON 05, KON 08, KON 3, MOKO 08, SIR 05, SIR 28 and TOKO 05 varied at 4 loci (data not shown). These populations thus should be well-suited for selecting individuals for a tree improvement program. The average levels of observed and expected heterozygosities were 0.273 and 0.238 respectively. Observed heterozygosities ranged from 0.24 to 0.30 while expected heterozygosity ranged from 0.22 to 0.26. The highest heterozygosities were found in Sirlawe and the lowest in Moulvoudaye, but overall the heterozygosities values for all of the populations were very close to one another (Table 6).
 
The Hardy-Weinberg Equilibrium (HWE) values for the 9 populations ranged from 0.75 to 1.00, with an average value across populations of 0.93 and overall value of 0.67 for all 255 samples (Table 6). These HWE values indicate that the populations are largely in genetic equilibrium and that the allele frequencies can be expected to be stable in subsequent generations. The case for genetic equilibrium is supported by the lack of linkage disequilibrium (LD) observed among alleles of the 8 loci across all populations. Although LD is not necessarily expected among only 8 loci, the lack of LD does confirm that the selected loci are likely to be performing as neutral and independent loci and thus appropriate for use in genetic diversity estimates.
 
The sampled F. albida populations in Cameroon displayed higher within population variation (98%) than among population variation (2%), as shown by the Fst values for  the  individual  SSR  loci  which  ranged  from 0.016 (1.6%) to 0.042 (4.2%) across the populations (Table 5). This finding was reinforced by the results of a pairwise comparison of FST values between the populations which resulted in a mean Fst value overall all comparisons of 0.02 and a range of Fst values between population pairs ranging from 0.00 to 0.07, with SD of 0.02.  (Table 7). An analysis of population structure using admixture detected 2 types of genotypes which were both widely distributed among all populations sampled (Figure 4). A principal component analysis (Figure 4) based on allelic variation among all 255 individuals was also unable to differentiate among the 9 populations of Faidherbia albida sampled in Northern Cameroon. Also, the FIS values were negative for most loci and ranged from -0.396 to 0.18.
 
 
 


 DISCUSSION

Eight  informative   microsatellite  markers  (SSRs)   were selected from the markers developed by Russell et al. (2014) for F. albida in tropical Africa to assess genetic diversity from populations in northern Cameroon for immediate application in seed collections for reforestation and agroforestry, and to initiate a breeding program. Phenotypic data were also collected and analyzed from the populations. It was found that there was higher within population than among population genetic variation, implying a high rate of gene flow between the Cameroon populations sampled. This is consistent with the extremely phenotypic variability found within individual populations, while overall the populations were morphologically quite similar. Genetic studies of other tropical fruit and timber species from Cameroon, using SSR markers, also indicated higher within population than among population variation (Benoit et al., 2011; Garcia et al., 2004), and similar results have been reported for Acacia senegal in Kenya (Omondi et al., 2010).  Analyses of isozyme loci showed that populations of   F.   albida   from   across  west  and  north  Africa  are
 
genetically diverse and are distinctly different from east African populations, which displayed a lower amount of genetic diversity (Joly et al., 1992; Harris et al., 1997; Dangasuk et al., 2002). In these previous studies, despite the high level of genetic diversity within the western and northern populations, within population diversity was found to be greater than among population diversity in this broad region (Harris et al., 1997). This may be attributable, in part, to exchange of seeds among farmers and transfer by animals during the nomadic life of herders in search of pasture (Hauser, 1994; Wickens, 1969).
 
The relatively low amount of genetic differentiation between populations of F. albida in the far north region of Cameroon has important implications for breeding studies.  From a practical standpoint, this result means that it is impossible to predict from genetic data which populations are most likely to provide superior sources  of breeding material.  Given that all of the populations examined in this study are genetically similar, in principle any population is a useful starting point for the derivation of improved varieties. However, the relatively large amount of genetic variation and phenotypic variation within each of the populations reveals substantial opportunities for selection and breeding for F. albida improvement at the population level.  Determining which populations and traits are best for breeding agronomically useful traits will require more detailed information, including which phenotypic traits segregate in families from different populations.  In contrast, even with the large number of samples genotyped, the FIS values were negative for most loci. Negative FIS values indicate an excess of heterozygotes in populations (Guries and Ledig, 1981). This suggests that F. albida populations in Cameroon are either subject to  high  selective  pressure, or arose from genetic bottlenecks from a relatively small number of founding individuals (Hedrick and Kalinowski, 2000).
 
In this study, the initial steps in establishing breeding and reforestation programs for F. albida in Cameroon have been accomplished through the collection of seed from natural populations and assessing of genetic and morphological variation among seedlings from these populations. The high levels of variation observed within all of the source populations provides ample opportunity for making great strides in trait improvement, while retaining genetic diversity, during the next steps of selecting trees with desirable genotypes and establishing breeding orchards.  The availability of the genome sequence of F. albida (Chang et al., 2018), will make it possible to identify many new polymorphic molecular markers useful for mapping quantitative trail loci linked to traits useful in agroforestry applications.  The genetic diversity results coupled with the genome sequence should enable the use of genome-wide marker assisted selection in Faidherbia --an approach that is widely used in the breeding of crop plants and has the potential to dramatically accelerate the discovery and improvement of trees useful for agroforestry (Alkimim et al., 2020; Grattapaglia, 2017; Ribaut et al., 2010; van Nocker and Gardiner, 2014; Watson, 2019; Zargar et al., 2015).  F. albida needs up to 12 years to flower (Barnes and Fagg, 2003), so breeding requires a long-term commitment on the part of both researchers and funding agencies. But, given the importance of F. albida in African agroforestry systems, it is an approach worth considering. Previous studies have shown that populations of F. albida from east and south Africa grow faster than populations from west Africa, but are also less drought tolerant than west African populations (Vandenbeldt, 1992; Dangasuk et al., 2006).  This suggests that populations derived from crosses between Cameroonian and east/south Africa populations could be an important source of novel, and potentially useful, varieties with improved growth and stress-tolerance attributes. 


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.


 ACKNOWLEDGEMENTS

The visit to Penn State University by Dr. Tchatchoua to conduct this research was funded by the Fulbright Visiting Scholar Fellowship program. The financial support for this work was provided by the Department of Biology at the University of Pennsylvania, The Schatz Center of Tree Molecular Genetics at Pennsylvania State University, and through the USDA National Institute of Food  and   Agriculture   Federal   Appropriations  under  Project PEN04532 and Accession number 1000326. All financial sources are gratefully acknowledged.



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