1. Introduction
Maize (
Zea mays L.) is the third most widely planted crop in the world after rice and wheat and the second most traded cereal after wheat [
1]. Globally, growth in production of maize is about 2.2% per annum, mainly through harvested area increase of 0.9% per annum and global average yield increase of 1.5% per annum [
2]. In sub-Saharan Africa (SSA), maize is an important staple crop for human consumption and provides at least 30 percent of the food calories for more than 50% of the population. Thus, its availability and affordability have been central to food security [
3] of countries in the sub-region [
4]. It is projected that if maize yield in SSA could be increased from the current 20% to 80% of the potential yield, then, SSA would attain self-sufficiency in 2050 [
5,
6]. Yield improvement in SSA is determined largely by the limited access of small-scale farmers to yield-enhancing inputs, such as improved seeds, fertilizers, machinery, and irrigation technologies [
7]. Even where improved varieties are available, the adoption has been poor due to the failure of new varieties to address farmers’ preferences or needs and their growing conditions [
8]. Often improved varieties are selected for high yield under optimal agronomic conditions. However, when grown by farmers in marginal production areas, they have failed to provide significant advantage over the farmers’ varieties and have not been adopted [
9].
Yield potential is location and year specific and highly controlled by temperature, solar radiation, water, nutrient supply, pest and diseases [
10]. Therefore, differences between yield potential and actual farm yield of a cultivar can only be achieved if the environmental factors are perfectly managed to enhance genetic potential of the cultivar. The three key production constraints responsible for yield reduction in SSA are soil nutrient constraints (44%), weeds (19%) including
Striga sp., and drought (18%) [
11]. Low soil nitrogen (low-N) stress alone is estimated to cause yield losses as high as 10–50% in SSA [
12,
13]. The problem of poor soil fertility, particularly low-N, could be alleviated by the addition of inorganic fertilizer as commonly done in high input agricultural systems in developed countries. However, fertilizer supply is limited and the cost is prohibitive for SSA farmers [
14]. As a result of high fertilizer costs, application rates in SSA are the lowest in the world [
15]. The high cost of fertilizer calls for the need to maximize nitrogen use efficiency (NUE) of maize varieties [
16] and encourage the use of nitrogen use efficient varieties, along with modest fertilizer use and other integrated soil fertility management practices to stabilize yields and increase the productivity of maize in SSA.
Striga hermonthica (Del.) Benth is an obligate parasitic weed commonly found in cereals in the savannas of West Africa and in the mid altitudes of East Africa. It causes yield losses of between 20–100% in maize [
2,
17].
Striga control methods commonly used in SSA include hand weeding, host plant resistance; chemical control and intercropping with catch or trap crops. The use of host plant resistance, i.e., maize varieties with the genes controlling the expression of the parasitic weed germination and development is considered the most preferred control method because it is sustainable, affordable and more environmentally friendly for resource poor farmers [
18,
19]. The integration of
Striga resistant maize varieties into
Striga management programs offers the most effective and sustainable control measure for the parasitic weed [
20]. Low soil fertility is also closely associated with
Striga hermonthica infestation [
21]. The simultaneous effects of
Striga and low-N can cause yield losses up to 100% [
22]. Maize production in SSA takes place mainly in rainfed systems. Maize yield is highly correlated with rainfall, which is important because drought is a defining feature of rainfed production environment. About 40% of Africa’s maize-growing area faces occasional drought stress, resulting in yield losses of 10–25%. About 25% of maize crop suffers from frequent drought, with losses of up to half the harvest [
23,
24]. Drought stress also hinders nutrient uptake. Maize grain yield is reduced by up to 80% under combined drought and low-N conditions [
25,
26]. Although the effects of uncertain and highly variable rainfall can be mitigated through the use of irrigation, SSA has the lowest level of irrigation development in the world. Only 4% of agricultural land in SSA is irrigated. As the effect of climate change advances and maize production continues to expand into marginal production areas, the effects of drought,
Striga and low-N stresses will remain major challenges in places where most farmers have limited capacity to invest in inputs [
27].
The savanna agro-ecologies of Ghana, representing the northern part of the country, have the greatest potential for increased maize production because solar radiation is high and incidence of pests and diseases is very low in these zones. However, maize productivity in northern Ghana is greatly constrained by drought, low soil fertility and
Striga infestation [
7,
28,
29]. Under field conditions, there are also often complex interactions among these stresses with more devastating effects on the yield of maize [
30,
31]. Investment in maize research is required to produce a new generation of improved multiple-stress tolerant varieties that are drought tolerant,
Striga resistant and nutrient use efficient in Ghana and Africa as a whole. The adoption of stress tolerant maize could generate USD 362 to USD 590 million within the maize production and consumption sector, which can seriously reduce poverty by 5% in SSA [
32].
Substantial progress in breeding for stress tolerant maize for African farmers has been achieved. Since 1990, the International Maize and Wheat Improvement Center (CIMMYT) and the International Institute of Tropical Agriculture (IITA) together with their global network of partners have developed several maize varieties (including breeding populations, open-pollinated varieties, hybrids and inbred lines) and relevant breeding techniques aimed at addressing major production constraints in Africa. These include drought, low-N and acid soil conditions,
Striga and insects [
33,
34]. The present study is part of broader research that focused on the utilization of new inbred lines developed by the West and Central Africa Collaborative Maize Research Network/International Institute of Tropical Agriculture (WECAMAN/IITA), for development of locally adapted maize hybrids with multiple-stress tolerance/resistance to
Striga and low-N for the savanna zones of Ghana, in particular and West and Central Africa (WCA), in general. The selected inbred lines included 100 early maturing white and yellow lines developed for drought/low-N and
Striga tolerance. Before hybrid development, there is a need to have adequate knowledge of the level of genetic diversity within the selected inbred lines for grain yield and other
Striga and low-N adaptive traits as well as the breeding value of the inbred lines to guide the selection of prospective parents of the desired hybrids. Since the majority of the inbred lines selected for this study are newly developed, there is little to no information on them with regards to these important genetic parameters, which would facilitate their use in hybrid development. To address these research gaps, a series of experiments were conducted to determine the genetic diversity, heterotic grouping, combining ability and heterosis for grain yield and other agronomic traits of the inbred lines under
Striga infestation, low-N and optimal growing conditions. The present study assessed the agronomic performance and trait associations of the inbred lines under optimal conditions,
Striga-infested and low-N environments to aid identification of superior lines through the use of multiple-trait selection index.
Genetic variation for stress adaptive traits is expressed differently at optimal and marginal environments. Thus, genes for adaptation to marginal environments can only be observed when genotype evaluation is conducted under sufficiently stressed conditions [
7,
35,
36,
37,
38]. The indirect selection of genotypes in optimal environments for performance in other contrasting environments is usually complicated by the presence of genotype by environment interaction (GEI). The presence of biotic (
Striga) and/or abiotic (Low-N and drought) stresses compound the GEI effects, probably due to the complexities in the genetics of resistance/tolerance of genotypes to stresses [
39]. Genotype by environment interaction due to the relative differences in the response of genotypes to contrasting environments reduces the correlation between phenotypic and genotypic values [
40] under stress environments. In maize, the relative effect of GEI on a genotype vary from one trait to the other with pronounced effects on quantitatively inherited traits such as grain yield. Most research outputs by CIMMYT have shown that variety selection based on grain yield alone under drought and low-N environments are usually inefficient because heritability of grain yield under stressed environments is low [
4]. Under such conditions, the use of secondary traits have improved selection efficiency in maize [
41]. According to Edmeades et al. [
41] an ideal secondary trait should be: genetically associated with grain yield under stress; highly heritable; genetically variable; cheap and fast to measure; stable within the measurement period, not associated with a yield penalty under non-stressed conditions observed at or before flowering, so that undesirable parents are not crossed and are reliable estimators of yield potential before final harvest [
35]. Traditionally, a selection index based on increased grain yield, reduced barrenness, reduced anthesis-silking interval (ASI), delayed leaf senescence, good plant and ear aspects is used to select for high yielding genotypes with tolerance to low-N and drought [
42,
43,
44]. For
Striga resistance improvement programs, a selection index which combines increased grain yield measured under
Striga-infested and
Striga-free environments, reduced
Striga damage, reduced number of emerged
Striga plants, good ear aspect and increased number of ears per plant (EPP) is used [
7,
45]. The use of these selection indices has been very successful in the past [
7,
46]. However, recent studies involving the same selection indices have reported inconsistent results. For instance, contrary to reports by Menkir and Akintunde [
43] and Badu-Apraku and Oyekunle [
47], results of Badu-Apraku et al. [
48] indicated that the stay green characteristic is not a reliable trait for selecting genotypes that are drought tolerant, while EPP and ASI are also unreliable characters for identifying low-N tolerant genotypes. The authors identified plant height, days to silking, and days to anthesis, which are not included in the low-N selection index as reliable for selecting early maturing inbred lines under low-N conditions. Reports by Badu-Apraku et al. [
48] and Badu-Apraku and Fakorede [
7] indicated that the number of emerged
Striga plants, which have a strong association with grain yield in late and intermediate maturity group of maize [
7,
45], have a weak phenotypic and genotypic correlations with grain yield in the early maturity group. Badu-Apraku and Fakorede [
7] found that after four cycles of S
1 family selection in an extra-early maturing population under
Striga infestation, grain yield was not correlated with other traits at C
0 but was significantly correlated with EPP,
Striga damage and the number of emerged
Striga plants in advanced cycles. A review of these contradictory results showed a trend dependent on the type of germplasm under selection, the kind of trait and the level of improvement already achieved in the desired germplasm. Since there is the possibility for every set of breeding lines to have unique trait associations, validation of long established secondary traits and assessment of the possible use of other traits in the selection of high yield and stress tolerant genotypes is relevant in breeding programs [
46]. The main objective of this study was to identify superior early maturing maize inbred lines that can contribute useful traits for hybrid development for stable production in low-N and
Striga infested environments, and also to be used for population improvement. The specific objectives of this study were to assess the relationship between grain yield and secondary traits of 100 white and yellow early maturing inbred lines, and also to assess the agronomic performance of the selected set of early maturing inbred lines based on multiple traits under optimal conditions,
Striga-infested and low-N environments.
4. Discussion
The observed significant genotypic, environment and GEI mean squares for most measured traits under
Striga infestation, low-N and optimal growing environments indicated that the test environments were unique and diverse, and provided important information on the inbred lines. It also indicated that there was adequate genetic variability among the inbred lines to allow for significant progress to be made in selection for
Striga resistance and low-N tolerance. Thus, there are potential parental lines for productive hybrid development for the targeted environments. Similar findings were reported by Badu-Apraku et al. [
59,
60] and Akaogu et al. [
61]. The significant interaction between genotype and environment for grain yield, days to anthesis and silking, plant height, ear aspect and ears per plant across the six test environments indicated that the expression of these traits will be inconsistent across environments and years. Therefore, the inbred lines should be evaluated under the different study environments across years to identify
Striga tolerant/resistant and/or low-N tolerant inbred lines with consistently favorable response to either one or both stresses [
60,
61,
62,
63,
64].
Nitrogen is the most important nutrient for the growth of maize, thus, the lack of it restricts plant growth, development and eventual yield. Based on the results of this study, traits, such as plant height, grain yield, ear aspect, days to silking and ears per plant, which were the most limited by nitrogen deficiency must be carefully considered when selecting low-N tolerant early maturing inbred lines. Several authors have reported similar effects of nitrogen stress on grain yield and its component traits [
65,
66,
67]. The observed delay in silking together with wide anthesis-silking interval under low-N might have induced barrenness, thus contributing to 36% grain yield reduction under low-N. The maize ear has a relatively weak sink capacity at flowering as a result; a reduction in nitrogen availability during flowering can reduce the flux of assimilates to the ear. This results in delay in silking, an increase in anthesis-silking interval, kernel abortion, barren plants and ultimately reduced grain yield [
65,
66].
Striga infestation significantly reduced grain yield and almost all yield components studied. On average, yield performance, ear aspect and ears per plant suffered a severe reduction of 49%, 26% and 21%, respectively under
Striga infestation relative to being under optimal conditions. This result suggested that ear aspect and ears per plant were key traits to consider when selecting early maturing
Striga resistant inbred lines for improved yield under
Striga-infested conditions. These results corroborated the findings of Adetimirin et al. [
68] whereby studies involving early maturing inbred lines and hybrids revealed that pre-flowering stress due to
Striga parasitism was higher than post-flowering stress and thus resulted in higher reduction of ears per plant (44%) than reductions for other yield components (12 ± 29%). The performance of the inbred lines with respect to key
Striga adaptive traits, such as
Striga damage syndrome rating and number of emerged
Striga plants, was outstanding. Generally, the inbred lines supported considerably fewer numbers of emerged
Striga plants of 9 and 21 plants per plot, respectively, at 8 and 10 WAP. The number of emerged
Striga plants recorded in this study are below the range of 21–31
Striga plants at 8 WAP and 24–39 emerged
Striga plants at 10 WAP reported by [
39,
47,
69]. The fewer number of emerged
Striga plants recorded in this study might have been influenced by the large number of test inbred lines with
Striga resistance genes derived from the germplasm with
Zea diploperennis genetic background. According to Lane et al. [
70], genotypes with genes from
Zea diploperennis restrict the penetration of its roots by
Striga plants and impair the development and survival of
Striga parasites. The selection index used to select superior inbred lines under
Striga-infested environment revealed that 49% of the inbred lines used in the present study might have possessed some level of tolerance and/or resistance to
Striga. They possessed desirable alleles for resistance to
Striga, which could have been used to develop more stable
Striga resistant hybrids and used also as sources of
Striga resistant alleles for population improvement.
Grain yield is a quantitative trait and is functionally related to yield components, particularly when evaluated under stress. Breeder’s knowledge of the degree of association among grain yield and its component traits is crucial, given that the selection of certain traits influences the behavior of other traits in crops [
46]. The results of the path analyses revealed that days to silking, ears per plot, days to anthesis and anthesis-silking interval had the highest direct effects on grain yield under optimal conditions, while ear aspect, plant height, days to silking, STRRAT2 and ears per plant were the traits with the greatest direct influence on grain yield under
Striga infestation. Under low-N, days to silking, ears per plant and days to anthesis were the most important traits with direct effects on grain yield. The results indicated that these traits could be used for indirect selection for improved grain yield in the respective environments. It is important to note that plant aspect, which is used in the IITA base index for selecting low-N tolerant early genotypes [
62,
71], did not have direct effect on grain yield. Furthermore, stay green characteristic considered as a key secondary trait in the identification of low-N tolerant genotypes [
35] had much weaker association with grain yield in the present study. The results of the present study were similar to the results of another study by Badu-Apraku et al. [
44], which revealed low correlation between the stay green characteristic and grain yield of extra-early inbred lines under both drought stress and low-N environments. Overall, the results of this study suggested that days to silking, ears per plant and plant height are more reliable traits for simultaneous selection of low-N tolerant early maturing inbred lines than stay green characteristic and plant aspect.
The path analysis also revealed that the direct and indirect effects of some of the measured traits on grain yield changed in magnitude and were inconsistent in direction across environments. The direct effect of days to anthesis on grain yield was moderately weak (0.49) under optimal conditions but approached 0.93 under low-N. The direct effect of ears per plant on grain yield also increased from −0.29 to 0.44 under optimal and low-N environments, respectively. Moreover, the indirect effect of days to silking on grain yield through days to anthesis and ears per plant also increased under low-N. These results are consistent with reports by Bänziger et al. [
35] who reported that correlation between grain yield and other yield components becomes stronger under stress. These results also showed a strong dependence of grain yield on flowering traits and hence, corroborated the findings of [
35,
39] on the effects of nitrogen deficiency on flowering, pollination and ear-setting processes of maize, and their consequent effects on yield of genotypes under nitrogen deficient environments. The positive correlation of days to anthesis and days to silking with grain yield under optimal growing conditions, the positive indirect effect of days to anthesis on yield through days to silking under optimal and low-N environments, as well as the positive direct effects of days to anthesis on grain yield under
Striga infestation, suggested that generally the inbred lines that matured late performed better than those that matured early in all the test environments. Sharifi and Namvar [
72] also found that yield potential of maize increased with increased days to anthesis and silking. Plant and ear heights usually have a positive association with grain yield in maize, therefore, the observed negative direct and indirect effects of plant and ear heights on grain yield under
Striga infestation is noteworthy. Theoretically, shorter plants have a lower amount of vegetative biomass, which reduces resource-use per plant for vegetative growth and maintenance, resulting in greater resource availability for grain production [
72].
The trait associations revealed by the genotype by trait biplots are consistent with the main patterns of trait associations revealed by the path coefficient analyses under optimal conditions, low-N and
Striga-infested environments. The results of the genotype by trait biplots showed that high yielding inbred lines in optimal growing conditions tended to be taller, had higher number of ears per plant and number of ears per plot as well as longer days to anthesis and silking. On the other hand, inbred lines with low grain yield had contrasting trait profile. In an earlier study involving extra-early maturing hybrids by Adu et al. [
73], higher grain yield was associated with increased plant height, number of plants and ears per plot as well as good ear aspect under optimal conditions. The inbred lines TZEI 124 and TZEI 344 possessed two or more of the desirable traits above and might have displayed the best performance under optimal conditions. Under low-N environments, high yielding inbred lines had taller plants and higher number of ears per plot. They were also earlier maturing. This result indicated that plant height, days to anthesis and ears per plot were invaluable traits in the selection for high grain yield under low-N environments. This result is consistent with the findings of Badu-Apraku et al. [
69]. Using genotype-by-trait biplot analyses, the authors [
69] found plant height and ear aspect as dependable traits for indirect selection for high yielding genotypes in nitrogen deficient and moisture-stressed environments. Under low-N, TZEI 35 had the best yield performance, were taller, and had the highest number of plants and ears harvested per plot. It could be invaluable resource in low-N breeding programs.
The pattern of associations among the traits identified under artificial
Striga infestation indicated that high yielding inbred lines in
Striga-infested environments had higher number of ears and plants per plot, shorter plants and were earlier maturing. High yielding inbred lines also had the lowest
Striga damage syndrome ratings at 10 WAP and best ear aspect. Poor yielding inbred lines had contrasting characteristics compared to those of the higher yielding lines. The strong association between grain yield and ear aspect indicated that it could be used to select for high yielding inbred lines in
Striga infested environments without sacrificing information on the inbred lines. The inbred line TZdEI 51 was identified as the best genotype for grain yield while TZEI 124 had the highest plant height and TZdEI 84 had the worst ear aspect and longest days to silking. The ABE biplot analysis identified days to anthesis, days to silking, plant height and number of ears harvested per plot as the most important traits with the greatest influence on grain yield of the inbred lines across optimal, low-N and
Striga-infested environments. Using these four traits and grain yield in the multi-trait selection index, TZEI 56, TZdEI 283, TZEI 18, TZEI 31, TZEI 35, TZEI 379, TZEI 476, TZEI 124 and TZEI 13 were identified as the most adapted inbred lines across the test environments. They may therefore be the most suitable parents for production of hybrids with improved grain yield across the three research environments. Generally, the promising inbred lines identified for each of the test environments could be the best choice of parental lines for developing hybrids with maximum expression of tolerance to low-N and
Striga infestation. However, since the per se performance of inbred lines is not a good indicator of the performance of the resulting hybrids, especially for grain yield [
74], there is the need to evaluate the inbred lines in hybrid combinations under the target environments to identify those with high combining abilities and better hybrid responses in the target environments.
A major objective of the present study was to identify early maturing maize inbred lines based on multiple traits under optimal, low-N and Striga-infested environments for hybrid development and population improvement. The high levels of genetic variability exhibited by the inbred lines for grain yield and other agronomic traits desirable for Striga resistance and low-N tolerance suggested that they would be useful in the development of superior high yielding hybrids as well as for population improvement.