Emmanuel Mrema , Hussein Shimelis Mark Laing Learnmore Mwadzingeni

1 University of KwaZulu-Natal/African Centre for Crop Improvement, Scottsville 3209, South Africa

2 Tumbi Agricultural Research Institute, Tabora, Tanzania

1. Introduction

Sorghum (Sorghum bicolour (L.) Moench, 2n=2x=20) is one of the key food security crops in sub-Sharan Africa(SSA) and Asia. In SSA, sorghum productivity is affected by Striga infestation, drought, birds, and storage pests.Striga hermonthica (Del.) Benth and Striga asiatica (L.)Kuntze are obligate root parasites that cause severe yield losses in sorghum and other cereal crops including rice(Oryza glaberrima Steudel and O. sativa L.), pearl millet(Pennisetum glaucum L.), and maize (Zea mays L.) (Riches 2003; Rodenburg et al. 2015).

Integrated Striga management (ISM) involving combined use of resistant varieties, biological control agents, cultural practices, and chemical control minimizes losses caused by the parasitic weeds (Hearne 2009). Breeding for Striga resistance in sorghum is an economically and environmentally sustainable management option (Ejeta 2007). Components of Striga resistance in sorghum include low haustorium initiation factor (LHF), mechanical barriers, inhibition of germ tube exoenzymes by root exudates, phytoalexin synthesis, incompatibility, antibiosis, insensitivity to Striga toxins, and Striga avoidance through various root growth habits (Wegmann 1996). Sorghum genotypes with low Striga germination stimulant or LHF have been reported to support few or no Striga attachments (Hess et al. 1992; Ejeta et al. 1997). The maximum germination distance (MGD)of Striga can effectively be screened for using the agar-gel assay developed by Hess et al. (1992). The technique involves spreading of preconditioned Striga seeds onto agar in Petri dishes followed by sowing of sorghum seeds and measuring of the maximum distance between sorghum rootlets and germinated Striga seeds. This is referred to as the MGD. Genotypes with a germination distance below 10 mm are classified as low germination stimulants offering considerable resistance against parasitism (Ejeta 2000).

The nature and magnitude of gene action influencing economic traits are key determinants of breeding procedures to follow. Several minor genes have been reported to be linked to enhanced germination of Striga (Vogler et al.1996). Haussmann et al. (1996) reported the influence of quantitative genetic variation and preponderance of additive genetic effects on the stimulation of S. hermonthica seed germination. Partial or complete dominant genes for Striga resistance were also reported on sorghum hybrids derived from crosses between resistant and susceptible parents(Obilana 1984). Estimation of these gene effects can effectively be achieved through generation mean analysis(GMA) based on the following six generations: female parent(P1), male parent (P2), F1progenies, F2segregants, and backcrosses to P1(BCP1) and P2(BCP2) (Anderson and Kempthorne 1954; Hayman 1958). The analysis is effective when the parents are divergent, possessing complementary and favourable alleles. It has been widely used to study gene action controlling Striga resistance in sorghum(Gamble 1962), maize (Badu-Apraku et al. 2013), and rice(Gurney et al. 2006). The mode of gene action controlling MGD of Striga in sorghum is not well documented, yet it is a necessary guide to Striga resistance breeding.

Development of Striga resistant sorghum genotypes that are compatible with Fusarium oxysporum f. sp. strigae(FOS), a biocontrol agent, is a novel ISM option against the obligate parasite (Rebeka et al. 2013). Pathogenic isolates of FOS are effective bio-herbicides, especially when integrated with other control practices (Rebeka et al. 2013).FOS is host specific, pathogenic, and highly destructive against Striga. It is also easy to mass-produce (Ciotola et al. 2000). Flowing seed treatment, the fungus proliferates in the rhizosphere of sorghum plants, and subsequently parasitizes Striga plants, stopping them from successfully attacking roots of the host plant (Rebeka 2007). Despite its potential, the effectiveness of FOS application to sorghum populations in Tanzania is yet to be explored. Selection of desirable parents, their crosses and backcross derivatives with reduced MGD and compatible with FOS may provide a foundation for ISM. This requires understanding of the genetic variability and inheritance of MGD of Striga among the selected genotypes (Mrema et al. 2017).

Promising sorghum genotypes with high FOS compatibility were identified under controlled evaluation conditions(Mrema et al. 2017). The lines possessed farmers’ preferred traits including adaptation to rain-fed conditions, while some had better yields and FOS compatibility (Mrema et al. 2016).Establishing the gene action influencing MGD of Striga among the selected lines could fill the current knowledge gap on the best breeding methodology to adopt in order to advance both Striga resistance and FOS compatibility.Therefore, this study aimed to determine the gene action controlling the MGD of S. hermonthica and S. asiatica from selected sorghum genotypes combined with FOS treatment using the generation mean analysis procedure.

2. Materials and methods

2.1. Plant materials and crosses

Twelve parents with high general and specific combining ability for the number of days to 50% flowering, seed yield per plant, and Striga resistance were used in this study (Mrema et al. 2017). Table 1 presents details of the studied genotypes. These lines were resistant to both S. hermonthica and S. asiatica and were compatible with FOS. Additionally, the lines harboured key traits preferred by farmers in semi-arid areas of Tanzania (Mrema et al.2016). The 12 parents were divided into two equal sets of females and males, which were crossed using a bi-parental mating design, producing six F1families. The families were subsequently selfed to produce F2families and remnant seed was preserved for evaluation. F1progeny families were backcrossed to their respective parents to generate backcross to parent one (BCP1) and backcross to parent two (BCP2) derivatives. These constituted the six basic generations, P1, P2, F1, BCP1, BCP2, and F2which weresubjected to generation mean analysis.

Table 1 Names and attributes of parental sorghum genotypes used for crosses

2.2. Bio-control agent and inoculum preparation

A pathogenic strain of F. oxysporum f. sp. strigae (FOS)originally isolated from sorghum fields infested with Striga in northeastern lowlands of Ethiopia was used as a bio-control agent for Striga management (Rebeka et al.2013). Taxonomic identification of FOS was confirmed by the Phytomedicine Department of Humboldt University in Berlin, Germany. The isolate was maintained on special nutrient agar (SNA) medium at –40°C. Pure Fusarium chlamydospores from cultures grown on potato dextrose agar (PDA) were sampled and mass-produced at Plant Health Products (Pty) Ltd., KwaZulu-Natal, South Africa and preserved by the Discipline of Plant Pathology, University of KwaZulu-Natal.

2.3. Experimental site

The six generations consisting of female parents (P1) and male parents (P2), F1progenies, F2segregants, backcrosses to P1(BCP1) and backcrosses to P2(BCP2) were evaluated to determine the MDG of S. hermonthica and S. asiatica and to evaluate their compatibility with FOS. The study was conducted at the Plant Pathology screen house facility and the laboratory of the African Seed Health Centre, Crop Science Department of Sokoine, University of Agriculture in Tanzania.

2.4. Experimental design and trial establishment

MGD of S. hermonthica and S. asiatica from sorghum genotypes was evaluated using an agar-gel assay developed by Hess et al. (1992) in two sets of experiments.One set involved S. hermonthica and the other set had S. asiatica, and both were with and without FOS treatments.The experiments were conducted using a split plot design with three replications. FOS treatment was the main-plot and genotypes were the sub-plots. Striga seeds were surface-sterilized by soaking in a 1% sodium hypochlorite solution for 5 min and then washing with distilled water using a filter paper on a funnel until the chlorine odour disappeared. Two layers of circular filter paper were placed in a Petri dish base of 9 cm diameter and wetted with distilled water. Discs with 5-mm filter paper were arranged on a moist paper in the Petri dish lid. Sterilized and dried Striga seeds were sprinkled onto the discs and the Petri dishes were covered with the lid. The Petri dishes were kept under dark conditions by covering them with aluminium foil. The Striga seeds were then incubated at 25°C for 15 days.The preconditioned Striga seeds were randomly sown into water agar in Petri dishes followed by planting a sterilised sorghum seed at the centre of each dish. Another set was sown with Striga and sorghum seeds dressed with 75 mg of FOS spores. Both sorghum and Striga seeds were left to germinate for 15 days and the MGD was determined at 5 days after germination.

2.5. Data analysis

Separate analysis of variance as well as test for normality and homogeneity of variances were conducted, followed by combined analysis of variance using the general linear model procedure (PROC GLM) in SAS ver. 9.3(SAS Institute 2011). The following model was used:Yijk=μ+Gi+Ej+G×E+rk(E)+eijk; where, Yijk, response on MGD of ith generation in jth FOS interaction of kth replication; μ,overall mean; Gi, generation mean; Ej, jth FOS interaction;G×E, generation×FOS interaction; rk, kth replication within FOS; and eijk, residual factor. Independent samples t-test was used to assess the significance of FOS treatment on MGD.

Data were subjected to GMA according to Mather and Jinks (1971). The PROC GLM and PROC REG procedures were performed using SAS as described by Kang (1994). The following genetic model was used:Y=m+aa+bd+a2aa+2abad+b2dd, where, a and b are the coefficients for a and d, respectively; Y, generation mean;m, mean of the F2generation as the base population and intercept value; a, additive genetic effect; d, dominance genetic effect; aa, additive×additive gene interaction effect; ad, additive×dominance gene interaction effect; dd,dominance×dominance gene interaction effect. A stepwise linear regression model was used to estimate the additive and dominance parameters. The parameters of the model were tested sequentially, starting with additive effects in order to determine the magnitude of additive, dominance,and epistatic genetic effects as described by Ceballos et al.(1998). The importance of the gene effects was estimated as the ratio of the sums of squares of each component over the total sums of square. Significance of the genetic estimates was determined by dividing the estimated parameter values with their standard errors and was considered significant if the value exceeded 1.96 (Singh and Chaudhary 1995).

3. Results

3.1. Analysis of variance for MGD of Striga among sorghum families, with and without FOS

The MGD of the two Striga species differed significantly(P＜0.01) among six generations of the six families evaluated with and without FOS application (Table 2). Under S. hermonthica infestation, most families interacted significantly with FOS application except for the crosses AS435×AS426 and 4567×AS426. Almost similar observations were made under S. asiatica infestation where the crosses 675×654, 1563×AS436, and 4567×AS424 showed significant interaction of the generation with FOS treatment.

3.2. Mean response of the tested sorghum population to FOS treatment under Striga infestation

Mean MGD and pair-wise contrasts among sorghum families evaluated, with and without FOS treatments, are presented in Table 3. There were significant differences among sorghum generation under infestation by the two Striga species with and without FOS. Application of FOS significantly reduced MGD in all other families except for AS435×AS426 and 4567×AS426 under S. hermonthica treatment, and in AS435×AS426 and 4567×AS426 under S. asiatica infestation. In addition, FOS-treated entries had shorter MGD as compared to their untreated controls.

3.3. Generation mean analysis of MGD of S. hermonthica and S. asiatica

Generation mean analysis for MGD of S. hermonthica and S. asiatica, with and without FOS, is presented in Table 4.Additive, dominance or epistatic genetic effects contributed significantly to the outcome of MGD among sorghum populations, evaluated with and without FOS. Additive genetic effects made highly significant contributions to MGD in both treatments for all families under infestation by thetwo Striga species. Under S. hermonthica infestation with FOS treatment, significant dominance genetic effects were recorded in families 675×654, 3424×3993, 1563×AS436,and 4567×AS424, while additive×additive gene effects were significant in all crosses due to FOS treatment.Additive×dominance interaction effects were significant contributors to genetic variation for MGD in AS435×AS426,4567×AS426, 3424×3993, 1563×AS436, and 3984×672 under S. hermonthica infestation with FOS treatment.Dominance×dominance interaction had significant influence on the expression of MGD for all tested populations, with and without FOS treatment. Under S. asiatica infestation and FOS treatment, significant contributions of dominance genetic effect were recorded in families 675×654,3424×3993, and 4567×AS424. Additive×dominance interaction effects contributed significantly to genetic variation for MGD in 1563×AS436 and 3984×672 under S. asiatica infestation with and without FOS treatment.Dominance×dominance interaction had significantly higher effects on MGD in both treatments.

Table 2 Mean squares and significance tests of the effect of Fusarium oxysporum f. sp. strigae (FOS) on germination distance between sorghum seed and the most distantly germinated Striga seed in six families of sorghum

Table 3 Mean maximum germination distance of Striga among six sorghum families with (+) and without (–) Fusarium oxysporum f. sp. strigae (FOS) application

Table 4 Mean squares and significance tests for the maximum germination distance between the sorghum seed and the most distantly germinated Striga seed evaluated with (+) and without (–) Fusarium oxysporum application in six families of sorghum

3.4. Relative contribution of the genetic effects on MGD of S. hermonthica and S. asiatica

The relative contributions of gene effects on MGD of the two Striga species in treatments with and without FOS are presented in Table 5. Additive, dominance, and epistatic genetic effect were significant, for most families with and without FOS treatment. Under S. hermonthica infestation,additive genetic effects contributed up to 29.97 and 33.61%of the total genetic variation for MGD, while under S. asiatica infestation, it contributed up to 31.89 and 29.02% of the total genetic variation with and without FOS, respectively,observed from the cross 1563×AS436. On the other hand,dominance and additive×dominance genetic effects made small contributions to the total genetic variation. Notably,high dominance genetic contributions of 20.05 and 31.87%were recorded under S. hermonthica infestation and 21.36 and 33.78% were recorded under S. asiatica infestation on the family 4567×AS424 with and without FOS, respectively.Further, under S. hermonthica infestation, additive×additive gene effects contributed up to 49.38 and 43.32% of the total genetic variation observed in the family 3424×3993 with and without FOS, respectively. Dominance×dominance interaction made higher contributions of 62.98 and 50.88%to the total genetic variation for MGD observed on the family AS435×AS426, with and without FOS in all tested families,respectively. Under S. asiatica infestation, these two families also had relatively high relative contribution of both additive×additive and dominance×dominance interactions.For both Striga species, additive×dominance interaction made little contribution to the total genetic variation for MGD in all tested families.

4. Discussion

4.1. Analysis of variance and mean response of the tested sorghum population to FOS treatment under Striga infestation

Significant differences in MGD of the two Striga species were observed among the six generations of the sorghum families evaluated with and without FOS application. Results indicated the presence of extensive variability for LFH and FOS compatibility, which could be useful for breeding. These findings concurred with Hess et al. (1992) who reported variation in MGD among sorghum genotypes evaluated with S. hermonthica infestation in an agar-gel assay. Existence of crosses, such as 675×654, 1563×AS436, and 4567×AS424,that interacted significantly with FOS application under both S. hermonthica and S. asiatica infestation could allow selection of transgressive segregates, as well as parental lines that have high general combining ability for combined Striga resistance and FOS compatibility. Mrema et al. (2017)recently reported presence of sorghum genotypes that are compatible with FOS. Variability in MGD of Striga observedacross generations in the current study indicates presence of variable gene interactions influencing the inheritance of MGD, hence, hybridisation and subsequent selection could produce improved varieties.

Table 5 Relative contribution of genetic effect (%) for the maximum germination distance between the sorghum seed and the most distant germinated Striga seed evaluated with (+) and without (–) Fusarium oxysporum f. sp. strigae (FOS) in six sorghum populations

Reduced MGD in FOS-treated entries confirms the fungus’ effectiveness as a bio-herbicide. FOS colonises sorghum roots and the rhizosphere such that when LHF is secreted, FOS degrades it to product that do not trigger Striga germination. This reduces stimulation of Striga germination by reducing LHF concentration, contributing to the antagonistic effects of FOS against the parasitic weed. Sorghum genotypes exhibiting MGD below 10 mm were reported to be Striga resistant (Ejeta 2000). These genotypes support few or no Striga (Ejeta et al. 1997).Therefore, selection of individual plants with desirable characteristics within families with a reduced MGD and with high compatibility with FOS would control Striga infestation(Ejeta 2000; Mrema et al. 2017). In this case, superior segregates exhibiting short MGD (≤10 mm) can best be selected from the F2generations where recombination frequency is the highest. The families AS435×AS426 and 4567×AS426, which exhibited no significant reduction of MGD following FOS application may be discarded from the breeding program since they may be susceptible to Striga attack and could be incompatible with the bio-control agent.

Currently, there are no reports of negative effects of Fusarium oxysporum f. sp. strigae on sorghum or related cereal crops. Recent studies indicated that FOS promotes the abundance of arbuscular mycorrhizal fungi in the rhizospheres of sorghum (Rebeka et al. 2013; Mrema et al.2017) and maize (Zimmermann et al. 2016; Shayanowako et al. 2017) enhancing agronomic performance of both crops. The host range of FOS is relatively narrow, which is presently confined to attacking three species of Striga including S. hermonthica, S. asiatica, and S. gesneroides parasitizing cereal and legume crops (Marley et al. 2005;Elzein and Kroschel 2006). However, it is not possible to rule out the possibility of emergence of mutant strains of FOS that can be pathogenic to sorghum or related crops.Therefore, further monitoring, evaluation, and knowledge would be valuable to detect any new pathogenic strains of F. oxysporum against sorghum or related cereal crops.Also, genomic diagnostic tools should be integrated with pathogenicity evaluation for early detection and to devise controlling strategies against any possible new pathogenic strains of FOS.

4.2. Generation mean analysis and relative contribution of the genetic effects on MGD of S. hermonthica and S. asiatica

The type and magnitude of gene action controlling key economic traits influence the response from selection and choice of the breeding methodology for quantitative traits. Additive gene action denotes heritable variation that can be transferred and traced to subsequent generations(Ceballos et al. 1998). Successful selection of Striga resistant and FOS compatible lines that combine additive genes contribute to favourable trait expression in a desirable direction. Sorghum families exhibiting predominantly dominance, over-dominance and/or epistatic gene effects can be ideal for selection of best specific combiners that result in transgressive segregates or for development of superior hybrids. In the case of dominance, dominant allele at each locus influence trait expression more strongly than the recessive allele, while epistatic gene interaction involves genes that can promote or suppress traits encoded by another gene(s) at different loci (Mather and Jinks 1971;Ceballos et al. 1998).

The significate contribution of additive, dominant, and epistatic genetic effects on the MGD of Striga among sorghum populations, with and without FOS implies that several breeding methodologies stretching from direct selection, hybridisation, and early generation selection could advance the trait. This allows for either effective transfer of additive genes from some of the parents evaluated or exploitation of heterosis exhibited by some families such as 675×654, 3424×3993, 1563×AS436, and 4567×AS424. Thus, chances are high for identifying unique parents and superior hybrids for commercialisation through crossing divergent but complementary parents. The family 1563×AS436 that exhibited high additive genetic contribution to the expression of MGD of the two Striga species could be key in passing on cumulative additive genes for MGD to next generations, and gain from selection from this family could be high. On the other hand, the family 4567×AS424 that exhibited high dominance genetic contributions to the expression of MGD under S. hermonthica infestation and S. asiatica infestation with and without FOS application could be a good source of parents for hybrid breeding to exploit heterosis. Overall, additive and non-additive genetic effects contributed highly to the total genetic variation for MGD. Additive gene effects and epistasis were reported to have higher contribution than dominance gene action in breeding for Striga resistance in sorghum (Kulkarni and Shinde 1985). Findings from the present study concur with the later study that reported Striga resistance to be controlled by both additive and non-additive gene action. This outcome suggests the possibility of fixing additive genes through recurrent selection.

5. Conclusion

The present study examined the genetic effects controlling the MGD among sorghum genotypes. Additive,additive×additive, and dominance×dominance genetic effects were responsible for most of the genetic variation present for MGD in the evaluated sorghum families.Dominance and additive×dominance genetic effects made minor contributions in the test populations. FOS treatment enhanced the expression of additive, additive×additive, and dominance×dominance genes, which had complementary effects on reducing MGD. FOS application increased contribution of additive genetic effects, raising the possibility of breeding for Striga resistant sorghum genotypes with FOS compatibility. This will allow deployment of superior sorghum cultivars with reduced MGD and compatible with the bioagent for ISM in Striga prone environments in Tanzania.Crosses 1563×AS436, 4567×AS424, and 3984×672 were identified to have reduced MGD in sets with S. asiatica and S. hermonthica through FOS application. These crosses are useful genetic resources to advance in ISM in the semi-arid regions of Tanzania.

Acknowledgements

The Alliance for a Green Revolution in Africa (AGRA) is gratefully acknowledged for financial support of the study through the African Centre for Crop Improvement (ACCI).Thanks are due to the Permanent Secretary, Ministry of Agriculture Livestock and Fisheries, and the Government of Tanzania, for giving study leave to the first author.

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