Inbred Selection for Increased Resistance to Kernel Contamination with Fumonisins
1
Misión Biológica de Galicia (CSIC), Carballeira 8, Salcedo, 36143 Pontevedra, Spain
2
Applied Mycology Unit, Department of Food Technology, Engineering and Science, University of Lleida, Agrotecnio-CERCA Center, Av. Rovira Roure 191, 25198 Lleida, Spain
*
Author to whom correspondence should be addressed.
Toxins 2023, 15(7), 444; https://doi.org/10.3390/toxins15070444
Submission received: 7 June 2023
/
Revised: 27 June 2023
/
Accepted: 3 July 2023
/
Published: 4 July 2023
(This article belongs to the Special Issue Toxins: 15th Anniversary)
Abstract
:In temperate world-wide regions, maize kernels are often infected with the fumonisin-producing fungus Fusarium verticillioides which poses food and feed threats to animals and humans. As maize breeding has been revealed as one of the main tools with which to reduce kernel contamination with fumonisins, a pedigree selection program for increased resistance to Fusarium ear rot (FER), a trait highly correlated with kernel fumonisin content, was initiated in 2014 with the aim of obtaining inbred lines (named EPFUM) with resistance to kernel contamination with fumonisins and adapted to our environmental conditions. The new released EPFUM inbreds, their parental inbreds, hybrids involving crosses of one or two EPFUM inbreds, as well as commercial hybrids were evaluated in the current study. The objectives were (i) to assess if inbreds released by that breeding program were significantly more resistant than their parental inbreds and (ii) to examine if hybrids derived from EPFUM inbreds could be competitive based on grain yield and resistance to FER and fumonisin contamination. Second-cycle inbreds obtained through this pedigree selection program did not significantly improve the levels of resistance to fumonisin contamination of their parental inbreds; however, most EPFUM hybrids showed significantly better resistance to FER and fumonisin contamination than commercial hybrids did. Although European flint materials seem to be the most promising reservoirs of alleles with favorable additive and/or dominance effects for resistance to kernel contamination with fumonisins, marketable new Reid × Lancaster hybrids have been detected as they combine high resistance and yields comparable to those exhibited by commercial hybrids. Moreover, the white kernel hybrid EPFUM-4 × EP116 exploits the genetic variability within the European flint germplasm and can be an alternative to dent hybrid cultivation because white flint grain can lead to higher market prices.
Key Contribution: This study contributes to cover the research gap in breeding maize to reduce kernel contamination with fumonisins. Effectiveness of pedigree selection procedure has been evaluated and promising hybrids developed from the released inbreds are shown as alternative to maize current commercial hybrids due to their increased resistance to kernel contamination with fumonisin and competitive grain yield.
1. Introduction
In temperate world-wide regions, maize kernels are often infected with the fumonisin-producing fungus Fusarium verticillioides, where the accumulation of fumonisins in the kernel above safety levels poses food and feed threats to animals and humans [1,2,3,4,5]. Several strategies can be managed to control kernel contamination with fumonisins and, among them, breeding has emerged as one of the most effective [6,7,8,9]. High kernel contamination with fumonisins is strongly associated with increased Fusarium ear rot (FER) disease caused by the fungus, as high genotypic correlation coefficients between the visual score for FER and fumonisin content have been reported across environments and genetic backgrounds [10,11,12,13]. Consequently, as fumonisin quantification is expensive and labor-consuming, FER is commonly used as the target trait in breeding programs to indirectly reduce fumonisin contamination.
Previous studies have reported that additive, dominance and epistatic effects are involved in maize resistance to FER [14,15,16,17]. Nevertheless, as additive effects are, in general, more important and stable than dominance effects are, and moderate to high genotypic correlation coefficients have been reported between inbred lines and testcrosses, breeding programs for increased resistance to FER have mainly focused on additive effects [11,18,19]. Introgressions from a resistant donor of resistance to FER (GE440) to a commercial inbred (FR1064) resulted in some inbred lines with improved disease resistance [20]. Similarly, a pedigree selection approach to breed inbred lines with increased resistance to FER and fumonisin accumulation resulted in maize genotypes more resistant to fumonisin accumulation in some environments [21]. Phenotypic recurrent selection for reduced FER and increased yield in the ReFus synthetic population, partially resistant to FER, attained significant gains for resistance to FER and indirectly for resistance to fumonisin accumulation in the population per se and in testcrosses [22]. Posteriorly, Butoto et al. [23] showed that genomic and phenotypic selection schemes applied to the ReFus population were similar and highly effective at reducing FER and fumonisin content. Based on the few reports on the effectiveness of breeding programs for increased resistance to FER, breeding efforts to reduce kernel contamination with fumonisins have been scarce and new initiatives are necessary to address farmers’ needs. Therefore, a pedigree selection program for increased resistance to FER was initiated by the breeding group of Misión Biológica de Galicia-CSIC in 2014 with the aim of obtaining inbred lines with resistance to kernel contamination with fumonisins. Because heritabilities for FER can be considerably reduced under natural conditions compared to artificial inoculation [12,24], selection was carried out under artificial inoculation conditions in order to achieve the highest efficacy. The main objectives of the current study were (i) to assess if inbreds released by that breeding program were significantly more resistant than their parental inbreds were and (ii) to examine if hybrids derived from EPFUM inbreds could be competitive based on grain yield and resistance to FER and kernel fumonisin contamination.
2. Results
In general, second-cycle inbred lines tended to improve resistance to FER and fumonisin contamination compared to their parental inbreds, although differences were not significant among either groups (defined in Table 1) or inbreds within groups (Figure 1 and Figure 2). The interactions of year × group and year × inbred (group) were also not significant.
Contrarily to inbreds, hybrids significantly differed for all traits, except for FER (Table 2). The interaction of year × hybrid was significant for days to silking and FER. Hybrids involving experimental inbreds presented lower fumonisin contents than commercial hybrids did, except EPFUM-3 × EP116 (Figure 3). Specifically, hybrids EPFUM-3 × EPFUM-8, EPFUM-3 × EPFUM-10, EPFUM-7 × EPFUM-1, EPFUM-7 × EPFUM-9, EPFUM-8 × EPFUM-1, EPFUM-8 × EPFUM-9, EPFUM-9 × EPFUM-2, EPFUM-10 × EPFUM-1, EPFUM-11 × EPFUM-1 and EPFUM-12 × EPFUM-2 were significantly less contaminated than was any commercial hybrid. Eight of these hybrids were crosses involving EPFUM inbreds developed from European flint materials (EPFUM-1 to 4). In addition, five hybrids involving experimental inbreds did not significantly differ for grain yield from the most productive commercial hybrid (Figure 4). These included EPFUM-6 × EPFUM-10, EPFUM-7 × EPFUM-9, and EPFUM-8 × EPFUM-9 corresponding to the Reid × Lancaster pattern, EPFUM-4 × EPFUM-9 to the European flint × Reid pattern, and the white-kernel hybrid EPFUM-4 × EP116 being a cross between two European flint inbreds. Hybrids EPFUM-8 x EPFUM-9 and EPFUM-7 × EPFUM-9 stood out for being among the best hybrids for grain yield and resistance to kernel fumonisin contamination. In addition, these hybrids presented good adaptation to cultivation in Northwestern Spain as days to shedding pollen ranged between 72 and 75 days and average kernel moisture ranged between 17.3 and 19.4 (Table 3).
The Pearson correlation coefficient between fumonisin content and FER was high among inbreds (N = 24, r2 = 0.76, p < 0.0001) and moderate among hybrids (Table 3). Pearson correlation coefficients between hybrid performance and mid-parent and heterosis estimates for FER and fumonisin content (Table 4) were computed with data collected on the 22 hybrids involving crosses between EPFUM inbreds (Table 5). High correlations were observed between heterosis and hybrid performance for FER and fumonisin content; meanwhile, correlation coefficients between hybrid performance and mid-parent estimates were low and not significant (Table 6).
3. Discussion
In the current study, second-cycle inbreds obtained through a pedigree selection program did not significantly improve the resistance to fumonisin contamination of their parental inbreds, but those parents were already the most resistant to fumonisin contamination among a diverse collection of inbred lines with more than 200 accessions [24]. This result did not seem to be a consequence of performing indirect selection using FER as the target trait because the correlation coefficient between FER and fumonisin content in the inbreds was high according to the previous literature [24,25,26]. More likely, selection based on single plant performance could be responsible for the weak resistance changes observed in the EPFUM inbreds compared to that of their parentals because low heritability estimates on an individual plant basis were reported for FER [26]. In this sense, an inbred selection scheme based on replicated family evaluation for FER resulted in a trend toward improved resistance to fumonisin accumulation, but with limited effectiveness [20].
On the other hand, most hybrids involving crosses among EPFUM inbreds showed better resistance to FER and fumonisin contamination than did commercial hybrids. Butoto et al. [24] suggested that breeders can effectively select inbreds for FER and FUM resistance, reserving the development and evaluation of topcross hybrids at the later stages of the breeding program. However, among the 22 hybrids developed from EPFUM inbreds, the correlation coefficients between the mid-parent value and hybrid performance for FER and fumonisin content were not significant; meanwhile, hybrid performance was highly correlated with mid-parent heterosis, suggesting that differences among these hybrids were driven predominantly by dominance and/or epistatic effects.
Among the best 10 hybrids for fumonisin content, eight were crosses between European flint inbreds and Lancaster or Reid inbreds, indicating that European flint materials are reservoirs of alleles with favorable additive and/or dominance effects. In agreement, Santiago et al. [25] studied the performance of a broad collection of inbred lines under inoculation with F. verticillioides and observed that flint inbreds had significantly (p < 0.10) less fumonisin content and FER than did the dent genotypes.
However, although hybrids with higher resistance to fumonisin contamination are highly desirable, resistance has to be accompanied by high grain yields to make hybrids commercially competitive. We could check that all commercial hybrids tested, with the exception of “Oldham”, showed higher yields but also higher fumonisin contamination. Within this context, Reid × Lancaster hybrids EPFUM-8 × EPFUM-9 and EPFUM-7 × EPFUM-9 were the most marketable hybrids because they combined high resistance and yields comparable to those exhibited by commercial hybrids. Hybrids EPFUM-6 × EPFUM-10, EPFUM-4 × EPFUM-9 and EPFUM-4 × EP116 could also be commercially interesting because these hybrids displayed kernel fumonisin contents that were significantly lower than those shown by the most productive commercial hybrid, “DA SPICIO”, but displayed comparable grain yields. EPFUM-4 × EP116 is a good example of heterosis within the European flint group as EPFUM-4 was derived from the cross of the inbred F575, developed from the French landrace “Millete Lauragais”, and the inbred EP65, developed from the Portuguese landrace “Regional de Fafe”; meanwhile, EP116 comes from a northern Spanish landrace, “Enano norteño × Vasco” [27]. The genetic variability within the European flint germplasm between EP116 and EPFUM-4 and their good adaptation to northwestern Spain, where these inbreds have been bred, have been capitalized on with the hybrid EPFUM-4 × EP116. Hybrid EPFUM-4 × EP116 can be an alternative higher-value specialty crop and add genetic variability to the current narrow-based commercial dent hybrids being grown [28]. The EPFUM-4 × EP116 hybrid would follow the western Europe × northern Spain pattern that in a previous study was represented by the landrace cross “Lazcano × Millette Lauragais” which was the most promising landrace cross across sites in that study [29]. In addition, another advantage of the hybrid EPFUM-4 × EP116 is its white kernel color, because flint white varieties are preferred for human consumption purposes in many places of the world [30,31]. In Europe, this hybrid could be particularly interesting in areas where the human consumption of maize as bread or polenta is common to reduce the associated risks of fumonisin contamination [32,33].
4. Conclusions
Second-cycle inbred lines from the three heterotic groups tested showed a non-significant improvement in resistance to FER and fumonisin contamination compared to their parental inbreds, probably due to the low inheritance of maize resistance to FER. Therefore, breeding schemes using replicated family evaluations for FER or genomic selection are the new approaches to be explored. However, hybrids involving crosses among the second-cycle lines showed lower contamination with fumonisins in comparison to commercial hybrids. This indicates the importance of dominance and epistatic factors for improving resistance to fumonisin contamination. European flint materials seem to be the most promising reservoirs of alleles with favorable additive and/or dominance for resistance to kernel contamination with fumonisins. The white kernel hybrid EPFUM-4 × EP116 exploits the genetic variability within the flint European germoplasm and can be a good alternative to dent hybrid cultivation because white flint grain can lead to higher market prices. In addition, new marketable Reid × Lancaster hybrids have been also identified, as they combined low fumonisin contamination and yields comparable to those exhibited by reference commercial hybrids.
5. Materials and Methods
5.1. Inbred Selection Program
Pedigree selection was initiated in 2014 using six F2 populations derived from crosses among inbreds chosen out of a broad collection of inbred lines based on their low values for FER and fumonisin content [25] (see details in Supplementary Table S1). F2 populations were obtained from crosses EP31 × EP39 and F575 × EP65 (involving inbreds from the flint European heterotic group), B93 × Oh43 and A670 × H95 (Lancaster group), and A630 × A635 and A654 × A666 (Reid group). Plant selection was performed among F2 plants, and family and plant within family selection was carried out during three subsequent self-crossing generations. Selection was performed under the kernel inoculation of the self-crossed ears. Ears were inoculated 7–14 days after self-pollination with a suspension of spores (106 spores/mL) of a strain of F. verticillioides deposited in the Culture Collection of the Misión Biológica de Galicia (CSIC-Spain) as MBG-1 [34]. This fungal isolate is an aggressive toxigenic isolate adapted to the local environment. At harvest, FER was estimated according to a 7-point scale (1 = no visible disease symptoms, 2 = 1–3%, 3 = 4–10%, 4 = 11–25%, 5 = 26–50%, 6 = 51–75%, and 7 = 76–100% of kernels exhibiting visual symptoms of infection) formulated by Reid and Zhu [35] and ears with the lowest values for FER (<3) were selected in each self-crossing generation resulting in the development of twenty-nine second-cycle F6 inbreds.
5.2. Inbred Evaluations
The second-cycle F6 inbreds and their parental inbreds were evaluated in 2019 for FER, and the two most promising second-cycle inbreds from each F2 together with parental inbreds were analyzed for fumonisin content. In 2021 and 2022, the evaluation focused on selected second-cycle inbreds (Table 1) and their parentals. Split-plot designs with two replicates were used for inbred line evaluation; main plots were assigned to inbred groups, with inbreds derived from the same cross constituting a group. Within each group, sub-plots were assigned to the different inbreds of the group. Each sub-plot consisted of a nine-hill row, with hills spaced 0.18 m apart within the row and 0.8 m between rows. Two kernels were sown in each hill to guarantee a plant density of approximately 70,000 plants ha−1 after thinning to one plant per hill. As natural kernel infection by F. verticillioides cannot guarantee sufficient and homogeneous inoculum levels, plants were artificially inoculated using a kernel inoculation technique [35,36]. In each row, 7–14 days after the silking date (the date on which more than 50% of plants in the row showed silks), all primary ears (nine) were inoculated with 2 mL of a spore suspension (106 spores per ml) of the fungal isolate of F. verticillioides used. Ears from each row were collected two months after inoculation and were individually rated for FER using the seven-point scale previously mentioned. Then, ears were dried at 35 °C for one week and shelled, and a representative kernel sample of approximately 60 g was ground and stored at 4 °C. Kernels were ground through a 0.75 mm screen in a Pulverisette 14 rotor mill (Fritsch GmbH, Oberstein, Germany). Ground samples were analyzed for total fumonisin content (fumonisins B1, B2, and B3) using a commercial ELISA kit (R-Biopharm Rhône Ltd., Glasgow, UK). The recovery rate of the test was approximately 60% with a mean coefficient of variation of approximately 8%; specificities for B1, B2, and B3 were 100%, and approximately 40% and 100%, respectively, and the detection limit was 0.125 mg kg−1. Extraction and preparation of samples, as well as test performance, were carried out as described in the kits.
5.3. Hybrid Evaluations
Attending to hybrid evaluation, twenty-seven crosses among second-cycle inbred lines and four commercial hybrids were tested in adjacent trials in 2021 and 2022. A complete randomized block design with two replications was used for each hybrid trial. The experimental plot consisted of a single 25-plant row, with the plants being spaced 0.18 m apart. The distance between adjacent rows was 0.8 m. In each row, 7–14 days after the silking date the primary ears of six plants were kernel-inoculated. Two months later, inoculated ears were harvested. The data recorded on each experimental plot were days to shedding pollen (number of days between sowing and the date on which 50% of plants had visible anthers); days to silking (number of days between sowing and the date on which 50% of plants had visible silks), kernel moisture, grain yield expressed in Mg ha−1, FER score for each inoculated ear using the visual 7-point scale and fumonisin content of the inoculated ears following the protocol explained above for inbred samples.
5.4. Statistical Analyses
An analysis of variance across years was performed for FER and fumonisin content recorded in inbred trials using the Proc Mixed procedure of SAS [37]. Group and inbred (group) were considered fixed effects and year, with replication and all interactions considered random effects. Similarly, an analysis of variance was computed with the same procedure for all data collected in hybrid trials, the hybrid being fixed and replication, and the year and the interaction year × hybrid being random. Least square mean comparisons among hybrids were performed using the Fisher’ protected least significant difference (LSD). In addition, mid-parent values and mid-parent heterosis were estimated for all crosses among the 12 released inbreds (22 hybrids). Mid-parent heterosis was computed as the difference between the hybrid and the mid-parent values divided by the mid-parent value. Pearson correlation coefficients among traits were performed with the procedure Proc CORR of SAS using average inbred and hybrid values.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/toxins15070444/s1, Table S1: Means of parental inbreds for fumonisin content (mg/kg) and Fusarium ear rot (FER) score in a previous two-year evaluation under inoculation with Fusarium verticillioides [25].
Author Contributions
A.B. conceived the study; R.S. took care of field experiments, data recording, and sample collection and preparation with the assistance of A.B. and R.A.M.; A.C. prepared the inoculum and performed inoculations; A.J.R. performed sample extractions and fumonisin quantification; A.B. performed statistical analyses of data; A.B. drafted the initial manuscript. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by subsequent coordinated projects financed by MCIU/AEI/FEDER, UE (RTI2018-096776-B-C21 and RTI2018-096776-B-C22, PID2021-122196OB-C21 and PID2021-122196OB-C22).
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
Data will be made available upon request.
Acknowledgments
A.C. acknowledges a PTA contract, PTA2018-015873-I, financed by MCIU/AEI/FSE+.
Conflicts of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.
References
- Furian, A.F.; Fighera, M.R.; Royes, L.F.F.; Oliveira, M.S. Recent advances in assessing the effects of mycotoxins using animal models. Curr. Opin. Food Sci. 2022, 47, 100874. [Google Scholar] [CrossRef]
- Chen, C.; Riley, R.T.; Wu, F. Dietary Fumonisin and Growth Impairment in Children and Animals: A Review. Compr. Rev. Food Sci. Food Saf. 2018, 17, 1448–1464. [Google Scholar] [CrossRef] [Green Version]
- Chen, J.; Wen, J.; Tang, Y.T.; Shi, J.C.; Mu, G.D.; Yan, R.; Cai, J.; Long, M. Research Progress on Fumonisin B1 Contamination and Toxicity: A Review. Molecules 2021, 26, 5238. [Google Scholar] [CrossRef] [PubMed]
- Voss, K.A.; Riley, R.T. Fumonisin Toxicity and Mechanism of Action: Overview and Current Perspectives. Food Saf. 2013, 1, 2013006. [Google Scholar] [CrossRef] [Green Version]
- Deepa, N.; Achar, P.N.; Sreenivasa, M.Y. Current Perspectives of Biocontrol Agents for Management of Fusarium verticillioides and Its Fumonisin in Cereals—A Review. J. Fungi 2021, 7, 776. [Google Scholar] [CrossRef]
- Eller, M.S.; Holland, J.B.; Payne, G.A. Breeding for improved resistance to fumonisin contamination in maize. Toxin Rev. 2008, 27, 371–389. [Google Scholar] [CrossRef]
- Santiago, R.; Cao, A.; Butron, A. Genetic factors involved in fumonisin accumulation in maize kernels and their implications in maize agronomic management and breeding. Toxins 2015, 7, 3267–3296. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Logrieco, A.; Battilani, P.; Leggieri, M.C.; Jiang, Y.; Haesaert, G.; Lanubile, A.; Mahuku, G.; Mesterhazy, A.; Ortega-Beltran, A.; Pasti, M.; et al. Perspectives on Global Mycotoxin Issues and Management From the MycoKey Maize Working Group. Plant Dis. 2021, 105, 525–537. [Google Scholar] [CrossRef] [PubMed]
- Braun, M.S.; Wink, M. Exposure, occurrence, and chemistry of fumonisins and their cryptic derivatives. Compr. Rev. Food Sci. Food Saf. 2018, 17, 769–791. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Löffler, M.; Miedaner, T.; Kessel, B.; Ouzunova, M. Mycotoxin accumulation and corresponding ear rot rating in three maturity groups of European maize inoculated by two Fusarium species. Euphytica 2010, 174, 153–164. [Google Scholar] [CrossRef]
- Löffler, M.; Kessel, B.; Ouzunova, M.; Miedaner, T. Covariation between line and testcross performance for reduced mycotoxin concentrations in European maize after silk channel inoculation of two Fusarium species. Theor. Appl. Genet. 2011, 122, 925–934. [Google Scholar] [CrossRef]
- Bolduan, C.; Miedaner, T.; Schipprack, W.; Dhillon, B.S.; Melchinger, A.E. Genetic variation for resistance to ear rots and mycotoxins contamination in early European maize inbred lines. Crop Sci. 2009, 49, 2019–2028. [Google Scholar] [CrossRef]
- Samayoa, L.F.; Cao, A.; Santiago, R.; Malvar, R.A.; Butron, A. Genome-wide association analysis for fumonisin content in maize kernels. BMC Plant Biol. 2019, 19, 166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Butron, A.; Reid, L.M.; Santiago, R.; Cao, A.; Malvar, R.A. Inheritance of maize resistance to gibberella and fusarium ear rots and kernel contamination with deoxynivalenol and fumonisins. Plant Pathol. 2015, 64, 1053–1060. [Google Scholar] [CrossRef] [Green Version]
- Boling, M.B.; Grogan, C.O. Gene action affecting host resistance to Fusarium ear rot of maize. Crop Sci. 1965, 5, 305–307. [Google Scholar] [CrossRef]
- Giomi, G.M.; Sampietro, D.A.; Velazco, J.G.; Iglesias, J.; Fernandez, M.; Oviedo, M.S.; Presello, D.A. Map overlapping of QTL for resistance to Fusarium ear rot and associated traits in maize. Euphytica 2021, 217, 81. [Google Scholar] [CrossRef]
- Netshifhefhe, N.E.I.; Flett, B.C.; Viljoen, A.; Rose, L.J. Inheritance and genotype by environment analyses of resistance to Fusarium verticillioides and fumonisin contamination in maize F-1 hybrids. Euphytica 2018, 214, 235. [Google Scholar] [CrossRef]
- Hung, H.-Y.; Holland, J.B. Diallel analysis of resistance to Fusarium ear rot and fumonisin contamination in maize. Crop Sci. 2012, 52, 2173–2181. [Google Scholar] [CrossRef] [Green Version]
- Padua, J.M.V.; Dias, K.O.D.; Pastina, M.M.; de Souza, J.C.; Queiroz, V.A.V.; da Costa, R.V.; da Silva, M.B.P.; Ribeiro, C.A.G.; Guimaraes, C.T.; Gezan, S.A.; et al. A multi-environment trials diallel analysis provides insights on the inheritance of fumonisin contamination resistance in tropical maize. Euphytica 2016, 211, 277–285. [Google Scholar] [CrossRef]
- Eller, M.S.; Payne, G.A.; Holland, J.B. Selection for reduced Fusarium ear rot and fumonisin content in advanced backcross maize lines and their topcross hybrids. Crop Sci. 2010, 50, 2249–2260. [Google Scholar] [CrossRef] [Green Version]
- Presello, D.A.; Pereyra, A.O.; Iglesias, J.; Fauguel, C.M.; Sampietro, D.A.; Eyherabide, G.H. Responses to selection of S-5 inbreds for broad-based resistance to ear rots and grain mycotoxin contamination caused by Fusarium spp. in maize. Euphytica 2011, 178, 23–29. [Google Scholar] [CrossRef]
- Horne, D.W.; Eller, M.S.; Holland, J.B. Responses to recurrent index selection for reduced Fusarium ear rot and lodging and for increased yield in maize. Crop Sci. 2016, 56, 85–94. [Google Scholar] [CrossRef]
- Butoto, E.N.; Brewer, J.C.; Holland, J.B. Empirical comparison of genomic and phenotypic selection for resistance to Fusarium ear rot and fumonisin contamination in maize. Theor. Appl. Genet. 2022, 135, 2799–2816. [Google Scholar] [CrossRef] [PubMed]
- Butoto, E.N.; Marino, T.P.; Holland, J.B. Effects of artificial inoculation on trait correlations with resistance to Fusarium ear rot and fumonisin contamination in maize. Crop Sci. 2021, 61, 2522–2533. [Google Scholar] [CrossRef]
- Santiago, R.; Cao, A.; Malvar, R.A.; Reid, L.M.; Butron, A. Assessment of corn resistance to fumonisin accumulation in a broad collection of inbred lines. Field Crop. Res. 2013, 149, 193–202. [Google Scholar] [CrossRef] [Green Version]
- Robertson, L.A.; Kleinschmidt, C.E.; White, D.G.; Payne, G.A.; Maragos, C.M.; Holland, J.B. Heritabilities and correlations of fusarium ear rot resistance and fumonisin contamination resistance in two maize populations. Crop Sci. 2006, 46, 353–361. [Google Scholar] [CrossRef]
- Revilla, P.; Soengas, P.; Malvar, R.A.; Cartea, M.E.; Ordas, A. Isozyme variation and historical relationships among the maize races of Spain. Maydica 1998, 43, 175–182. [Google Scholar]
- Revilla, P.; Malvar, R.A.; Cartea, M.E.; Soengas, P.; Ordas, A. Heterotic relationships among European maize inbreds. Euphytica 2002, 126, 259–264. [Google Scholar] [CrossRef] [Green Version]
- Revilla, P.; Boyat, A.; Alvarez, A.; Gouesnard, B.; Soengas, P.; Ordas, A.; Malvar, R.A. Heterotic patterns among French and Spanish maize populations. Maydica 2006, 51, 525–535. [Google Scholar]
- Malvar, R.A.; Revilla, P.; Moreno-Gonzalez, J.; Butron, A.; Sotelo, J.; Ordas, A. White maize: Genetics of quality and agronomic performance. Crop Sci. 2008, 48, 1373–1381. [Google Scholar] [CrossRef]
- CIMMYT. White Maize: A Traditional Food Grain in Developing Countries: A Joint Study / by the Basic Foodstuffs Service, FAO Commodities and Trade Division and the Economics Program, International Maize and Wheat Improvement Center; International Maize and Wheat Improvement Center; Food and Agriculture Organization of the United Nations: Rome, Italy, 1997. [Google Scholar]
- Lino, C.M.; Silva, L.J.G.; Pena, A.; Fernandez, M.; Manes, J. Occurrence of fumonisins B-1 and B-2 in broa, typical Portuguese maize bread. Int. J. Food Microbiol. 2007, 118, 79–82. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pilu, R.; Cassani, E.; Sirizzotti, A.; Petroni, K.; Tonelli, C. Effect of flavonoid pigments on the accumulation of fumonisin B1 in the maize kernel. J. Appl. Genet. 2011, 52, 145–152. [Google Scholar] [CrossRef]
- Cao, A.; Butron, A.; Ramos, A.J.; Marin, S.; Souto, C.; Santiago, R. Assessing white maize resistance to fumonisin contamination. Eur. J. Plant Pathol. 2014, 138, 283–292. [Google Scholar] [CrossRef] [Green Version]
- Reid, L.M.; Hamilton, R.E.; Mather, D.E. Screening Maize for Resistance to Gibberella Ear Rot; Agriculture and Agri-Food Canada: Ottawa, ON, Canada, 1996; p. 62. [Google Scholar]
- Mesterhazy, A.; Lemmens, M.; Reid, L.M. Breeding for resistance to ear rots caused by Fusarium spp. in maize—A review. Plant Breed. 2012, 131, 1–19. [Google Scholar] [CrossRef]
- Statistical Analysis Systems Institute, SAS, version 9.1; SAS Institute Inc.: Cary, NC, USA, 2008.
Figure 1.
Least square means (±standard error) of the 12 released second-cycle inbreds (EPFUM) and their parents for fumonisin content evaluated across three years. Inbred derived from the same cross and inbreds involved in that cross are in the same color (brown for European flint, green for Lancaster and blue for Reid inbreds).
Figure 1.
Least square means (±standard error) of the 12 released second-cycle inbreds (EPFUM) and their parents for fumonisin content evaluated across three years. Inbred derived from the same cross and inbreds involved in that cross are in the same color (brown for European flint, green for Lancaster and blue for Reid inbreds).
Figure 2.
Least square means (±standard error) of the 12 released second-cycle inbreds (EPFUM) and their parents for Fusarium ear rot (FER) evaluated across three years. Inbred derived from the same cross and inbreds involved in that cross are in the same color (brown for European flint, green for Lancaster and blue for Reid inbreds).
Figure 2.
Least square means (±standard error) of the 12 released second-cycle inbreds (EPFUM) and their parents for Fusarium ear rot (FER) evaluated across three years. Inbred derived from the same cross and inbreds involved in that cross are in the same color (brown for European flint, green for Lancaster and blue for Reid inbreds).
Figure 3.
Means of the hybrids for fumonisin content evaluated in two years under inoculation with Fusarium verticilllioides. Means with the same letter did not significantly differ at the 0.05 probability level. Commercial hybrids are in orange.
Figure 3.
Means of the hybrids for fumonisin content evaluated in two years under inoculation with Fusarium verticilllioides. Means with the same letter did not significantly differ at the 0.05 probability level. Commercial hybrids are in orange.
Figure 4.
Means of the hybrids for grain yield evaluated in two years under inoculation with Fusarium verticilllioides. Means with the same letter did not significantly differ at the 0.05 probability level. Commercial hybrids are in orange.
Figure 4.
Means of the hybrids for grain yield evaluated in two years under inoculation with Fusarium verticilllioides. Means with the same letter did not significantly differ at the 0.05 probability level. Commercial hybrids are in orange.
Table 1.
Released maize inbred lines (EPFUM) and their parental inbreds evaluated in three years under inoculation with Fusarium verticillioides.
Table 1.
Released maize inbred lines (EPFUM) and their parental inbreds evaluated in three years under inoculation with Fusarium verticillioides.
| Group 1 | Released Inbred | Parent 1 | Parent 2 | Heterotic Group | Kernel Color |
|---|---|---|---|---|---|
| EP31 × EP39 | EPFUM-1 | EP31 | EP39 | European flint | yellow |
| EP31 × EP39 | EPFUM-2 | EP31 | EP39 | European flint | yellow |
| F575 × EP65 | EPFUM-3 | F575 | EP65 | European flint | white |
| F575 × EP65 | EPFUM-4 | F575 | EP65 | European flint | white |
| B93 × Oh43 | EPFUM-5 | B93 | Oh43 | Lancaster | yellow |
| B93 × Oh43 | EPFUM-6 | B93 | Oh43 | Lancaster | yellow |
| A670 × H95 | EPFUM-7 | A670 | H95 | Lancaster | yellow |
| A670 × H95 | EPFUM-8 | A670 | H95 | Lancaster | yellow |
| A630 × A635 | EPFUM-9 | A630 | A635 | Reid | yellow |
| A630 × A635 | EPFUM-10 | A630 | A635 | Reid | yellow |
| A654 × A666 | EPFUM-11 | A654 | A666 | Reid | yellow |
| A654 × A666 | EPFUM-12 | A654 | A666 | Reid | yellow |
1 Second-cycle inbreds derived from the same cross are clustered in the same group as well as are the inbreds involved in that cross.
Table 2.
Z- and F-values of the analysis of variance of 28 hybrids involving crosses between the released EPFUM inbred lines and four commercial hybrids evaluated for resistance and agronomical traits in two years under inoculation with Fusarium verticillioides.
Table 2.
Z- and F-values of the analysis of variance of 28 hybrids involving crosses between the released EPFUM inbred lines and four commercial hybrids evaluated for resistance and agronomical traits in two years under inoculation with Fusarium verticillioides.
| Source of Variation | Days to Shedding Pollen | Days to Silking | Kernel Moisture | Yield | FER | Fumonisin Content |
|---|---|---|---|---|---|---|
| Random (Z-value) | ||||||
| Year | 0.68 | 0.69 | 0.68 | 0.68 | 0.18 | |
| Replication (year) | 0.95 | 0.94 | 0.75 | 0.88 | 0.40 | |
| Year × Hybrid | 1.37 | 1.88 * | 0.50 | 0.53 | 2.81 ** | |
| Residual | 5.57 ** | 5.57 ** | 5.62 ** | 5.51 ** | 5.53 ** | 6.82 ** |
| Fi×ed (F-value) | ||||||
| Hybrid | 18.40 ** | 16.95 ** | 2.56 ** | 6.56 ** | 1.44 | 2.68 ** |
*, ** Z- or F-values significant at 0.05 and 0.01 probability levels, respectively.
Table 3.
Least square means of 28 maize hybrids involving crosses of EPFUM inbreds and four commercial hybrids for days to shedding pollen, Fusarium ear rot (FER) and kernel moisture evaluated at harvest for two years.
Table 3.
Least square means of 28 maize hybrids involving crosses of EPFUM inbreds and four commercial hybrids for days to shedding pollen, Fusarium ear rot (FER) and kernel moisture evaluated at harvest for two years.
| Hybrid | FER (1–7) | Kernel Moisture (%) | Days to Shedding Pollen |
|---|---|---|---|
| Ambassad | 2.9 a | 17.1 e–g | 73.2 bc |
| Da SPICIO | 3.5 a | 17.3 e–g | 72.5 c–e |
| PR36W66 | 3.2 a | 18.0 d–g | 75.8 a |
| Oldham | 3.3 a | 15.9 fg | 63.3 l |
| EPFUM-1 × EPFUM-6 | 2.5 a | 23.0 ab | 69.3 g–i |
| EPFUM-1 × EPFUM-9 | 2.7 a | 19.8 c–e | 70.8 d–h |
| EPFUM-2 × EPFUM-5 | 2.2 a | 19.9 c–e | 65.8 kj |
| EPFUM-3 × EP116 | 3.4 a | 19.1 c–f | 71.5 c–f |
| EPFUM-3 × EP117 | 2.9 a | 19.2 c–f | 69.3 g–i |
| EPFUM-3 × EPFUM-10 | 2.4 a | 18.1 d–g | 72.0 c–e |
| EPFUM-3 × EPFUM-8 | 1.8 a | 19.0 d–f | 72.8 cd |
| EPFUM-3 × PB40 | 3.0 a | 19.1 c–f | 70.8 d–h |
| EPFUM-4 × EP116 | 3.2 a | 19.1 d–f | 71.0 d–g |
| EPFUM-4 × EP117 | 2.9 a | 19.4 c–e | 69.5 f–i |
| EPFUM-4 × EPFUM-9 | 2.6 a | 17.8 d–g | 71.8 c–e |
| EPFUM-4 × PB40 | 2.8 a | 19.6 c–e | 72.0 c–e |
| EPFUM-5 × EPFUM-1 | 2.3 a | 19.3 c–e | 64.5 kl |
| EPFUM-5 × EPFUM-10 | 3.4 a | 19.6 c–e | 70.5 e–h |
| EPFUM-6 × EPFUM-10 | 3.4 a | 19.1 d–f | 71.3 c–g |
| EPFUM-6 × EPFUM-2 | 2.1 a | 23.8 a | 68.8 ih |
| EPFUM-7 × EPFUM-1 | 2.0 a | 17.3 e–g | 67.8 ij |
| EPFUM-7 × EPFUM-9 | 1.8 a | 17.3 e–g | 75.3 ab |
| EPFUM-8 × EPFUM-1 | 1.7 a | 20.5 b–d | 68.0 i |
| EPFUM-8 × EPFUM-9 | 2.4 a | 19.4 c–e | 71.8 c–e |
| EPFUM-9 × EPFUM-2 | 2.5 a | 15.4 f | 68.3 i |
| EPFUM-9 × EPFUM-6 | 2.5 a | 22.2 a–c | 72.5 c–e |
| EPFUM-10 × EPFUM-1 | 2.0 a | 19.7 c–e | 65.3 kl |
| EPFUM-10 × EPFUM-8 | 3.1 a | 18.7 d–f | 70.5 e–h |
| EPFUM-11 × EPFUM-1 | 2.3 a | 19.5 c–e | 64.8 kl |
| EPFUM-11 × EPFUM-5 | 2.9 a | 19.8 c–e | 67.8 ij |
| EPFUM-12 × EPFUM-2 | 2.3 a | 19.9 c–e | 64.3 kl |
| EPFUM-12 × EPFUM-8 | 3.3 a | 19.3 c–e | 68.3 i |
Means in the same column followed by the same letter did not significantly differ at the 0.05 probability level.
Table 4.
Mid-parent and heterosis estimates for FER and fumonisin content computed with data collected on the 22 hybrids involving crosses between EPFUM inbreds.
Table 4.
Mid-parent and heterosis estimates for FER and fumonisin content computed with data collected on the 22 hybrids involving crosses between EPFUM inbreds.
| Hybrid | Mid-Parent 1 | Mid-Parent Heterosis | ||
|---|---|---|---|---|
| FER | Fumonisin | FER | Fumonisin | |
| EPFUM-1 × EPFUM-6 | 2.70 | 22.0 | −0.0859 | −0.4575 |
| EPFUM-1 × EPFUM-9 | 2.72 | 21.0 | −0.0035 | −0.1263 |
| EPFUM-2 × EPFUM-5 | 3.38 | 31.3 | −0.3592 | −0.1684 |
| EPFUM-3 × EPFUM-8 | 2.08 | 8.0 | −0.1203 | −0.3218 |
| EPFUM-3 × EPFUM-10 | 2.52 | 11.6 | −0.0397 | −0.3192 |
| EPFUM-4 × EPFUM-9 | 2.36 | 16.8 | 0.1113 | −0.2488 |
| EPFUM-5 × EPFUM-1 | 2.87 | 21.2 | −0.2169 | −0.3788 |
| EPFUM-5 × EPFUM-10 | 2.69 | 18.9 | 0.2567 | 0.1870 |
| EPFUM-6 × EPFUM-2 | 3.20 | 32.1 | −0.3485 | −0.7021 |
| EPFUM-6 × EPFUM-10 | 2.50 | 19.7 | 0.3490 | −0.0550 |
| EPFUM-7 × EPFUM-1 | 2.41 | 13.5 | −0.1716 | −0.3829 |
| EPFUM-7 × EPFUM-9 | 2.09 | 15.0 | −0.1416 | −0.4670 |
| EPFUM-8 × EPFUM-1 | 2.42 | 13.5 | −0.3125 | −0.4359 |
| EPFUM-8 × EPFUM-9 | 2.10 | 15.0 | 0.1322 | −0.7858 |
| EPFUM-9 × EPFUM-2 | 3.23 | 31.1 | −0.2380 | −0.7006 |
| EPFUM-9 × EPFUM-6 | 2.36 | 23.5 | 0.0582 | 0.1750 |
| EPFUM-10 × EPFUM-1 | 2.86 | 17.1 | −0.3000 | −0.5773 |
| EPFUM-10 × EPFUM-8 | 2.24 | 11.2 | 0.3635 | −0.0184 |
| EPFUM-11 × EPFUM-1 | 3.09 | 30.1 | −0.2707 | −0.7407 |
| EPFUM-11 × EPFUM-5 | 2.91 | 31.9 | −0.0133 | −0.5124 |
| EPFUM-12 × EPFUM-2 | 3.96 | 36.0 | −0.4220 | −0.7896 |
| EPFUM-12 × EPFUM-8 | 2.84 | 20.0 | 0.1487 | −0.1797 |
1 The mid-parent estimate was calculated as the average performance across years of both inbred parents of the hybrid. The mid-parent heterosis estimate was calculated as the difference between the hybrid mean and the mid-parent value divided by the mid-parent value.
Table 5.
Pearson correlation coefficients among traits recorded in the 32 hybrids across two years.
| Days to Silking | Kernel Moisture | Yield | FER | Fumonisin Content | |
|---|---|---|---|---|---|
| Days to shedding pollen | 0.95 ** | −0.11 | 0.64 ** | 0.22 | 0.28 |
| Days to silking | −0.06 | 0.51 ** | 0.23 | 0.23 | |
| Kernel moisture | −0.10 | −0.24 | −0.21 | ||
| Yield | 0.29 | 0.32 | |||
| FER | 0.66 ** |
** significant at 0.01 probability level.
Table 6.
Pearson correlation coefficients between hybrid performance and mid-parent and heterosis estimates for Fusarium ear rot (FER) and fumonisin content computed with data collected on the 22 hybrids involving crosses between EPFUM inbreds.
Table 6.
Pearson correlation coefficients between hybrid performance and mid-parent and heterosis estimates for Fusarium ear rot (FER) and fumonisin content computed with data collected on the 22 hybrids involving crosses between EPFUM inbreds.
| Mid-Parent 1 | Heterosis | |||
|---|---|---|---|---|
| r2 | p-Value | r2 | p-Value | |
| FER | 0.02 | 0.94 | 0.80 | <0.0001 |
| Fumonisin content | 0.29 | 0.20 | 0.76 | <0.0001 |
1 The mid-parent estimate was calculated as the average performance across years of both inbred parents of the hybrid. The mid-parent heterosis estimate was calculated as the difference between the hybrid mean and the mid-parent value divided by the mid-parent value.
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MDPI and ACS Style
Santiago, R.; Ramos, A.J.; Cao, A.; Malvar, R.A.; Butrón, A. Inbred Selection for Increased Resistance to Kernel Contamination with Fumonisins. Toxins 2023, 15, 444. https://doi.org/10.3390/toxins15070444
AMA Style
Santiago R, Ramos AJ, Cao A, Malvar RA, Butrón A. Inbred Selection for Increased Resistance to Kernel Contamination with Fumonisins. Toxins. 2023; 15(7):444. https://doi.org/10.3390/toxins15070444
Chicago/Turabian StyleSantiago, Rogelio, Antonio J. Ramos, Ana Cao, Rosa Ana Malvar, and Ana Butrón. 2023. "Inbred Selection for Increased Resistance to Kernel Contamination with Fumonisins" Toxins 15, no. 7: 444. https://doi.org/10.3390/toxins15070444
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