1. Introduction
Maize (
Zea mays L.) is an economically important annual cereal crop that is predicted to become the most important cereal crop in the world by 2025 [
1]. The current global yield of maize is about 1.1 billion tons and production is projected to increase to over 1.4 billion tons by 2030 [
1,
2]. It is estimated that 50% of the total population of West and Central Africa (WCA) depends on maize as a staple food while a large proportion of the maize produced annually is used as raw materials for various alcoholic beverages, poultry and the livestock industries [
3,
4]. As a staple food crop of the sub-region, maize plays an important role in combating malnutrition. The normal endosperm maize has about 71% starch compared to the quality protein maize (QPM) which has 46% lysine and 66% tryptophan in addition to the 71% starch. The two amino acids supply provide about 70–73% of the requirement of the human body [
4,
5,
6]. Early studies by Akuamoah- Boateng [
7] on infants fed with QPM porridge revealed reduced growth stunting, fewer sick days, and healthier growth statistics than those fed with normal endosperm maize. Other studies by Mbuya et al. [
8] and Panda et al. [
9] reported that QPM could replace soybean in poultry feed production which could reduce the cost of animal feed.
In addition to the agro-ecological advantage, the savannas of SSA contribute to high maize productivity through high incoming solar radiation and reduced incidence of pests and diseases due to prevailing low humidity and low night temperature conditions [
4,
10]. However, tropical soils have low levels of organic matter and available nitrogen, resulting in nutrient-depleted soils which cause grain yield losses of up to 80% [
11,
12]. Thus, resource-poor farmers constituting a large proportion of the maize producers in SSA can hardly afford mineral fertilizers due to the high cost of nitrogen-based fertilizers as well as the general non-availability of fertilizers [
4,
13]. Furthermore, climate change threatens the goal of achieving global food security and could have severe socio-economic consequences globally [
14]. With the fast-increasing world population, maize production is expected to be significantly affected by the adverse impacts of climate change and could lead to a global food crisis with major impacts, particularly in SSA [
15,
16,
17,
18]. Although maize is well adapted and substantially utilized in the savannas of SSA, the concurrent incidence of abiotic stresses such as drought and high temperature during flowering could reduce the photosynthetic rate, accelerate leaf senescence, induce kernel abortion and ultimately cause drastic yield losses [
19,
20]. The combination of the two stresses could lead to a grain yield loss of more than 90% during flowering and grain filling in maize [
10,
21,
22,
23,
24].
According to Neate [
25], 40% of the maize production areas in SSA will be unsuitable for cultivation of the available maize germplasm due to the threat posed by CDHS as well as lack of tolerance to low-nitrogen by 2030. A major challenge of maize breeders of the present generation is to develop maize cultivars with CDHS and low-nitrogen tolerance for the agro-ecological zones of SSA [
4,
15]. A number of early and extra-early maturing maize QPM hybrids with tolerance to
Striga, low-nitrogen and drought stress have been developed by the International Institute of Tropical Agriculture Maize Improvement Program (IITA-MIP) and commercialized in West and Central Africa (WCA) [
4,
26]. However, very little information is available on QPM maize hybrids with tolerance to CDHS. While several studies have been conducted on the improvement of maize varieties for tolerance to drought and heat stress separately, Cairns et al. [
27] highlighted that tolerance to both stresses separately did not confer tolerance to CDHS and concluded that drought and heat stresses in maize were genetically different from tolerance to the individual stresses. This calls for the need for the development and commercialization of hybrids with CDHS and low-nitrogen tolerance for SSA to mitigate the adverse effects of these stresses on farmers, particularly the resource-poor farmers.
Maize breeding efforts in recent years have recorded significant successes in identifying lines that could be used as tolerance donors for breeding of cultivars with CDHS tolerance. Cairns et al. [
15] identified donor lines among CIMMYT and IITA inbred lines possessing high levels of tolerance to CDHS that could be used for the development of outstanding hybrids. In another study, Meseka et al. [
21] assessed the level of tolerance in existing drought tolerant hybrids under CDHS and reported an appreciable level of tolerance among the hybrids. Similarly, Nelimor et al. [
22] assessed early maize landraces from Ghana, Burkina-Faso and Togo, and identified accessions that could be invaluable donors of tolerant alleles for hybrid development under CDHS conditions. However, very few reports are available on the genetic action regulating grain yield and other agronomic traits under CDHS.
Breeding of early white QPM maize hybrids with tolerance to CDHS and the information on the gene action involved in the inheritance, the combining ability and heterotic patterns of inbred lines in the IITA-MIP are crucial to their successful use for hybrid development and production [
26,
28]. A recent study by Chiuta and Mutengwa [
24] reported the preponderance of the non-additive gene action in the inheritance of grain yield of subtropical QPM inbreds under CDHS suggesting that hybrid development could be adopted as an efficient and effective breeding strategy for the development of tolerant cultivars [
26]. Contrarily, Nasser et al. [
29] studied the combining ability of early maturing yellow maize inbreds and reported the importance of the additive gene action over the non-additive gene action in the inheritance of grain yield under CDHS. The inconsistencies in the reports on the relative importance of the additive and non-additive gene action in the inheritance of grain yield and other traits call for the need for further studies to confirm the type of gene action controlling grain yield and other agronomic traits in the newly developed early maize QPM inbred lines in the IITA-MIP. Additionally, several studies have reported the preponderance of additive gene action over non-additive gene action in the inheritance of grain yield under low-nitrogen conditions [
12,
30,
31,
32]. Contrarily, studies by Makumbi et al. [
33] and Badu-Apraku et al. [
26] reported that non-additive gene action conditioned the grain yield of maize hybrids under low-nitrogen, while Noelle et al. [
34] reported that both additive and non-additive genetic action conditioned grain yield when soil nitrogen was low. These conflicting reports by researchers could be due to the severity of the low-nitrogen environments or the germplasm used in the studies. Consequently, there is a need to evaluate the gene action conditioning the inheritance of grain yield and other important traits under low-nitrogen environments using the newly developed early white QPM inbred lines of the IITA-MIP.
The availability and use of early white QPM hybrids with tolerance to CDHS and low-nitrogen conditions would be more sustainable for smallholder farmers in nitrogen-depleted areas of SSA where low levels of agricultural inputs are utilized and there is simultaneous incidence of drought and heat stresses [
4]. Therefore, the objectives of this study were to: (a) investigate the gene action conditioning grain yield and other agronomic traits of early white QPM inbred lines under CDHS, low-nitrogen, as well as optimal growing environments; (b) group the inbred lines into heterotic groups using the heterotic grouping method based on the combining ability of multiple traits (HGCAMT) and identify inbred and single-cross testers; (c) assess the performance of the QPM inbred lines in hybrid combinations and identify high yielding and stable QPM hybrids under CDHS, low-nitrogen and across test environments.
3. Discussion
The significant genotypic variation (
p < 0.01) observed among the early QPM hybrids under low-nitrogen, CDHS, optimal and across test environments indicated that considerable genetic variation existed among the genotypes to facilitate accelerated gains from selection under contrasting environments. The observed significant differences for environments among the QPM hybrids revealed that each research environment was unique in terms of climatic and edaphic conditions which further suggested the need for extensive evaluations in contrasting environments. The significant genotype by environment interactions observed for grain yield and other measured traits under low-nitrogen, CDHS, optimal environments and across test environments implied that the hybrids responded distinctively to the environments. This emphasized that the environments were different and that the performance of the hybrids would not be consistent in different environments. Similar findings were reported by Ertiro et al. [
12], Badu-Apraku et al. [
26], Ifie et al. [
30] under low-nitrogen and Meseka et al. [
21], Nelimor et al. [
22] under CDHS environments
Very low heritability estimates were obtained for grain yield, anthesis and silking interval, and stay green characteristic of the QPM hybrids under low-nitrogen and tassel blasting under CDHS environments suggesting that selection based on phenotypic expression of these traits would be ineffective in achieving significant genetic gains. Contrary to the results of the present study, Meseka et al. [
21] and Nelimor et al. [
22,
23] reported relatively moderate heritability estimates for grain yield under CDHS. Additionally, moderate to high repeatability estimates recorded for most measured traits indicated the reliability of the data for the measured traits in the present study [
4].
Partitioning the QPM hybrids into genetic components, significant GCAm and GCAf mean squares were observed for grain yield and other measured traits under low-nitrogen environments implied that additive gene action was more important in the inheritance of grain yield and other measured traits under low-nitrogen. Similar findings were reported by Ifie et al. [
30], Annor and Badu-Apraku [
31], Obeng-Bio et al. [
11], and Abu et al. [
32] on the preponderance of the additive gene action over the non-additive gene action in the inheritance of grain yield under low-nitrogen environments. Contrarily, studies by Makumbi et al. [
33], and Neolle et al. [
34] reported non-additive gene action to be more important in the inheritance of grain yield under low-nitrogen environments.
Under CDHS environment conditions, the significant GCAf and SCA mean squares for grain yield and other measured traits, except for GCAm for grain yield, ASI, plant height, plant and ear aspects implied that both the additive and the non-additive gene actions were involved in the inheritance of grain yield and other measured traits under CDHS. Furthermore, the preponderance of SCA variances over GCA variances for grain yield indicated that non-additive gene action was more important than the additive and that the non-additive gene action was more important for the inheritance of grain yield traits under CDHS. This result is consistent with the findings of Chiuta and Mutengwa [
24] who reported the preponderance of the non-additive gene action over the additive in the inheritance of grain yield under CDHS environments. Contrarily, Nasser et al. [
29] reported the preponderance of the additive gene action over the non-additive in the inheritance of grain yield under CDHS environments.
The significant GCAm, GCAf and the SCA mean squares for grain yield and other measured traits under optimal environments, except the GCAm for ASI and ear rot as well as the GCAf and the SCA for grain yield and ear rot, indicated that both the additive and the non-additive gene action were important in the inheritance of grain yield and other measured traits under optimal environments. The larger GCAm and GCAf mean squares for grain yield compared to the SCA mean squares, indicated that the additive gene action was more important in the inheritance of grain yield under optimal environments. This result is consistent with the findings of Makumbi et al. [
33], Noelle et al. [
34], Oyekale et al. [
37], and Chiuta and Mutengwa [
24] who reported that additive gene action controlled grain yield under optimal conditions.
The non-significant SCA mean squares recorded for the stay-green characteristic under low-nitrogen and CDHS environments indicated that the non-additive gene action was not important in the inheritance of the stay-green characteristic in this study. This result is similar to the findings of Badu-Apraku et al. [
38] and Ifie et al. [
30] who reported non-significant SCA mean squares for the stay-green characteristic under low-nitrogen conditions. However, the significant GCAm mean squares observed for the stay green characteristic under low-nitrogen and the significant GCAm and GCAf mean squares observed for the stay green characteristic under CDHS, indicated that there were variations in the expression of the QPM inbreds as parents in hybrid combinations for the stay green characteristic under CDHS conditions. Similar results were reported by Annor and Badu-Apraku [
31] and Badu-Apraku et al. [
26] who reported significant GCAm and GCAf effects for stay green characteristic under drought and low-nitrogen environments. The implications of these results are that recurrent selection methods should be the most effective for increasing the frequency of favourables alleles in a breeding population for the development of synthetic varieties. Contrarily, the preponderance of non-additive gene action implied that hybrid development should be employed under CDHS to exploit heterotic potentials of the QPM inbred lines. The differences in the results of the different authors could be attributed to differences in the germplasm studied, the statistical model employed, the severity of stress levels imposed and the experimental mating design used [
4,
26].
The non-significant GCAm × environment (E), GCAf × environment (E) and SCA × environment (E) interactions observed for measured traits except the GCAm × E for ASI and the GCAf × E for grain yield under low-nitrogen conditions, indicated that the performance of the parental lines were consistent across the low-nitrogen environments. This result is in agreement with the findings of Derera et al. [
39] and Oyekale et al. [
37] who reported non-significant GCAm × E, GCAf × E and SCA × E interactions for grain yield under drought and low-nitrogen environments. Contrarily, Annor and Badu-Apraku [
31] and Badu-Apraku et al. [
26] reported significant GCAm × E, GCAf × E and SCA × E interactions for grain yield and other measured traits of extra-early and early QPM inbreds under low-nitrogen stress. Similarly, Obeng-Bio et al. [
11] reported significant GCAm × E, GCAf × E and SCA × E interactions for grain yield and other traits in early pro-vitamin A (PVA) QPM inbred lines under low-nitrogen. The significant GCAf × E interaction for grain yield suggested that the GCA effects associated with the female parents were not the same across the low-nitrogen environments.
Under low-nitrogen environments, comparable contributions of GCAm and GCAf sum of squares were observed for grain yield and other measured traits except ASI, indicating that both maternal and paternal effects were equally important in the inheritance of the measured traits of the hybrids. Similar studies by Ifie et al. [
30], Annor and Badu-Apraku [
31], Obeng-Bio et al. [
11] reported no significant differences in the contribution of both GCAm and GCAf (paternal and maternal effects) for grain yield and other measured traits under low-nitrogen. However, GCAm for ASI was larger than GCAf, suggesting the importance of paternal effects in the inheritance of anthesis and silking interval. The larger GCAf sum of squares relative to GCAm sum of squares observed under CDHS environments for grain yield and plant aspect indicated the greater importance of cytoplasmic effect on the inheritance of grain yield and plant aspect. Also, ears per plant had significantly larger GCAf sum of squares than the GCAm sum of squares indicating that maternal effects conditioned prolificacy and that the parental lines with significant and positive GCAf effects for ears per plant should be used as the female parents in hybrid production to ensure prolificacy under CDHS.
According to Girma et al. [
40], the information on the combining of ability of parental lines for a trait is useful in determining the contribution of the parental lines to their progenies in hybrid combinations. In other words, parental lines with significant GCA effect for a trait under a stress condition has high probability of transferring the favourable alleles for the trait to progenies in hybrid combinations and such parental lines could be useful in the development of outstanding hybrids [
4]. The observed significant and positive GCAm and GCAf effects for grain yield recorded by TZEQI 6 under low-nitrogen environments indicated that the parental line would transfer favourable alleles to the progeny when used either as a female or a male parent. Similarly, the significant and positive GCAm effects for grain yield recorded by TZEQI 106, TZEQI 113, TZEQI 158, TZEQI 188 and TZEQI 6 under low-nitrogen environments suggested that these inbred lines when used as male parents, would transfer favourable alleles for grain yield to their progenies under low-nitrogen environments. A similar inference could be made for the inbred TZEQI 210 which displayed significant and positive GCAf effects for grain yield. Additionally, the observed significant and positive GCAm effects for grain yield by TZEQI 113 and TZEQI 216 implied that both parental lines would transfer favourable alleles to their progenies when used as male parents under CDHS environment. In addition, the significant and negative GCAf effects observed for stay green characteristic was an indication that TZEQI 6, TZEQI 113, TZEQI 132, TZEQI 158 and TZEQI 219 would contribute favourable alleles to their progenies for delayed senescence or prolonged stay green characteristic, increased photosynthesis and assimilate production under low-nitrogen conditions.
Using the HGCAMT grouping method, the 24 QPM inbred lines were classified into four heterotic groups. Interestingly, crosses between inbred lines from different heterotic groups displayed higher heterosis across stress environments indicating the effectiveness of the grouping method. The heterotic groups identified by the HGCAMT method across environments would increase the chances of developing outstanding early maturing QPM hybrids and synthetics with CDHS and low-nitrogen tolerance for commercialization in SSA. Additionally, heterotic populations could be developed by recombining QPM inbred lines from the same heterotic group and improving the population through recurrent selection methods [
41].
Based on the criteria proposed by Pswarayi and Vivek [
36] for identifying inbred and single-cross testers, inbred line TZEQI 6 with significant and positive GCAm and GCAf effects for grain yield was identified as a tester under low-nitrogen environment conditions, suggesting that TZEQI 6 was a good combiner and could be used either as a male or a female parent in the development of high yielding hybrids and for grouping of other inbred lines under low-nitrogen environments. This result confirmed the earlier report by Badu-Apraku and Fakorede [
4] who identified TZEQI 6 as a tester. It was therefore, not surprising that TZEQI 6 was involved in the following outstanding hybrid combinations: TZEQI 6 × TZEQI 228, TZEQI 113 × TZEQI 6, TZEQI 6 × TZEQI 210 and TZEQI 6 × TZEQI 219. Hybrid TZEQI 113 × TZEQI 6 was identified as a single-cross tester and could be used for the development of three-way and double-cross hybrids [
26].
An important objective of this study was to identify the most outstanding hybrids under each and across test environment conditions. The QPM hybrids TZEQI 6 × TZEQI 219 and TZEQI 6 × TZEQI 228 were identified as the most outstanding across CDHS and low-nitrogen environments. These hybrids could be useful in the development of early maturing multiple-stress tolerant three-way QPM hybrids for commercialization in SSA.
The significant genotype by environment interaction observed for grain yield under CDHS, low-nitrogen and across test environments in the present study justified the use of the GGE biplot to identify high yielding and stable QPM hybrids for commercialization in SSA. From the “which-won-where” view of the GGE biplot, hybrids TZEQI 241 × TZEQI 216, TZEQI 6 × TZEQI 210, TZEQI 39 × TZEQI 44 (check) and TZEQI 6 × TZEQI 55 (check) were identified as the highest yielding in low-nitrogen, optimal and CDHS environments, respectively. Additionally, the mean yield vs. stability of the GGE biplot view identified TZEQI 39 × TZEQI 44 (check) as the highest yielding and TZEQI 210 × TZEQI 188 as the most stable QPM hybrids across test environments. These results suggested that these hybrids would display superior performance in nitrogen depleted, drought prone environments without compromising grain yield.
Because of the quantitative nature of grain yield and the low heritability recorded for grain yield under the stress environment conditions used in this study, selection using grain yield alone without other agronomic traits would be ineffective [
42]. Therefore, there was the need to examine the interactions among the secondary traits and their relative contribution to grain yield for effective selection. Under low-nitrogen conditions, plant and ear aspects were identified as the most important secondary traits contributing to the observed variations in grain yield, thus suggesting their reliability as secondary traits for selection under low-nitrogen environments. In an earlier study, Badu-Apraku et al. [
43] using sequential path analysis, identified plant and ear aspects as the first order traits with direct contribution to grain yield under low-nitrogen environments. Additionally, the stay green characteristic contributed indirectly to grain yield through both plant and ear aspects, indicating its reliability as a secondary trait thus justifying its inclusion in the selection base index under low-nitrogen environments. Under CDHS environments, the direct contributions of both ear aspect and ear height to grain yield indicated that they were the major determinants of grain yield. Plant aspect contributed indirectly to grain yield through the two first order traits (ear aspect and ear height), indicating its importance in the selection of genotypes under CDHS environments. Similarly, both ear aspect and ear height had direct contributions to grain yield across test environments, implying that they were the major contributors to grain yield. These results justified the inclusion of plant and ear aspects in the selection index under both stress conditions. Additionally, this suggested the need to revisit the issue of the inclusion of ear height as one of the secondary traits in the selection index under stress environments. However, increasing ear height is not desirable because it is associated with stalk lodging. Therefore, in the IITA-MIP plant and ear heights are usually pegged and not allowed to increase.