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Quality Protein Maize Based on Reducing Sulfur in Leaf Cells

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Quality Protein Maize Based on Reducing Sulfur in Leaf Cells | INVESTIGATION Quality Protein Maize Based on Reducing Sulfur in Leaf Cells Jose Planta and Joachim Messing1 Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854 ABSTRACT Low levels of the essential amino acids lysine (Lys) and methionine (Met) in a maize-based diet are a major cost to feed and food. Lys deficiency is due to the abundance of Lys-poor proteins in maize kernels. Although a maize mutant, opaque-2 (o2), has sufficient levels of Lys, its soft kernel renders it unfit for storage and transportation. Breeders overcame this problem by selecting quantitative trait loci (QTL) restoring kernel hardness in the presence of o2, a variety called Quality Protein Maize (QPM). Although at least one QTL acts by enhancing the expression of the g-zein proteins, we could surprisingly achieve rebalancing of the Lys content and a vitreous kernel phenotype by targeting suppression of g-zeins without the o2 mutant. Reduced levels of g-zeins were achieved with RNA interference (RNAi). Another transgenic event, PE5 expresses the Escherichia coli enzyme 39-phosphoadenosine-59-phosphosulfate reductase involved in sulfate assimilation, specifically in leaves. The stacked transgenic events produce a vitreous endosperm, which has higher Lys level than the classical opaque W64Ao2 variant. Moreover, due to the increased sulfate reduction in the leaf, Met level is elevated in the seed. Such a combination of transgenes produces hybrid seeds superior to classical QPMs that would neither require a costly feed mix nor synthetic Met supplementation, potentially creating a novel and cost-effective means for improving maize nutritional quality. KEYWORDS High-lysine maize; high-methionine maize; quality protein maize N many developing countries, maize serves as an important Therefore, a lot of research efforts has been expended on Isource of nutrition in human and animal diets. Cereals like genetic improvements to the amino acid balance of maize maize are limiting in essential amino acids (EAAs) Lys, Met, kernels, either through conventional breeding or the use of and tryptophan (Trp), whereas legume crops like soybean are recombinant DNA technology. deficient in Met. Therefore, corn is usually supplemented with The bulk of proteins in mature maize kernels, prolamins, soybean and synthetic free Met to provide a balanced amino called zeins in maize, possess an amino acid imbalance to- acid diet for animal feed. Although humans could live on a diet ward proline, glutamine, alanine, and leucine residues. Zeins of beans and corn, they cannot consume synthetic free Met, are classified into four distinct classes of a- (19- and 22-kDa), which, as a racemic substance, would not be allowed for b- (15-kDa), g- (16-, 27-, and 50-kDa), and d-zeins (10- and health reasons. Met as a limiting nutrient had been demon- 18-kDa) and coalesce into discrete spherical structures called strated in the effects of methionine fortification of a soy protein bodies (PBs) (Kim et al. 2002). Mature PBs have a isolate-based formula in infant feeding. Normal infants fed shell of g-andb-zeins surrounding the core of a-zeins. The soy isolate-based formula fortified with methionine had sig- 27-kDa g-zein controls PB initiation, whereas the 50-kDa nificant weight gain compared to infants fed not supple- g-zein plays a significant role in PB expansion, the bulk of mented soy isolate-based formula (Fomon et al. 1979). which is driven by the 19-kDa a-zein. The 22-kDa a-zein provides structural support in packaging the 19-kDa a-zein Copyright © 2017 by the Genetics Society of America (Guo et al. 2013). On the other hand, the nonzein protein doi: https://doi.org/10.1534/genetics.117.300288 fraction in the endosperm (glutelins, globulins, and albu- Manuscript received September 13, 2017; accepted for publication October 17, 2017; mins)isrelativelybalancedintheiraminoacidcomposition published Early Online October 20, 2017. Supplemental material is available online at www.genetics.org/lookup/suppl/doi:10. (Prasanna et al. 2001). This abundance of zeins effectively 1534/genetics.117.300288/-/DC1. dilutes the contribution of other endosperm proteins to the 1Corresponding author: Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, 190 Frelinghuysen Rd., Piscataway, NJ 08854. E-mail: kernel Lys and Trp contents. Therefore, alterations in the [email protected] accumulation of zeins have led to the identification of Genetics, Vol. 207, 1687–1697 December 2017 1687 mutants with altered nutritional quality. For instance, in- kernel genotypes have higher Lys and Met contents than the creased accumulation of the b-, g-, and d-zeins relative to o2 mutant. Moreover, PE5 with RNAi targeting of g-zeins themoreabundanta-zeins (Supplemental Material, Table could potentially be a preferred QPM variety because of S1 in File S1) has raised the sulfur (S) amino acid contents higher Lys and Met levels and their dominance for introgres- of kernels and their nutritional value (Planta et al. 2017). sion into elite lines. Reduction of a-zeins either through transcriptional regula- tion (e.g., loss of O2 transcription factor), or a transgene Materials and Methods that reduces their transcript accumulation through RNA in- Genetic stocks terference (RNAi), result in more nutritionally balanced en- dosperm proteins. The a-, g-, and b2RNAi transgenic plants were from our One of the zein-reduction mutants, the recessive o2 mu- laboratory stocks, and have been described elsewhere (Wu tant, has about a 50% reduction in zeins (Tsai et al. 1978), and Messing 2010, 2011; Wu et al. 2012). Both the gRNAi and approximately double the amount of Lys compared to and bRNAi are homozygous for A654-Dzs10, a nonfunctional normal genotypes (Mertz et al. 1964). It primarily affects allele of the 10-kDa d-zein gene from the inbred A654. The the synthesis of a-zeins. The 22-kDa a-zeins are reduced to bRNAi plant used for crosses is homozygous for the RNAi a very low level, whereas the 19-kDa a-zeins are also re- transgene as all kernel progenies tested positive for bRNAi duced, but to a lesser extent (Jones et al. 1977). The o2 genotyping, whereas the gRNAi is hemizygous, as about half mutant, aside from a reduced Lys-poor zein content, has a of the tested kernel progenies from crosses with gRNAi had compensating increase in the levels of Lys- and Trp-rich non- the RNAi transgene. aRNAi, on the other hand, is in a Hi-II zein proteins. However, its soft and starchy endosperm makes A 3 B hybrid background, and is hemizygous for the RNAi it susceptible to fungi and insect infestation, both in storage transgene. The hybrid genotype Hi-II A 3 B was used for and in the field (NRC 1988). Identification of o2 modifiers maize transformation. (mo2s) function as suppressors that can restore the normal The transgenic event PE5 was backcrossed twice to the kernel phenotype in the presence of o2, resulting in a new high-Met inbred line B101 prior to being crossed with the type of maize germplasm, known as quality protein maize RNAi lines. It expresses the Escherichia coli enzyme 39-phos- (QPM) (Prasanna et al. 2001). phoadenosine-59-phosphosulfate reductase, designated as Alternatively, transforming maize with an RNAi transgene EcPAPR (Martin et al. 2005), driven by the PepC promoter targeting the a-zeins also enhances levels of Lys and Trp in (Sattarzadeh et al. 2010). EcPAPR is involved in assimilatory maize kernels (Segal et al. 2003; Huang et al. 2004, 2006). sulfate reduction, and maize plants expressing this enzyme The observed increase in Lys and Trp in the a-zein-reduced shows increased kernel Met content when used as the mater- kernels was also due to the replacement of the Lys-poor zeins nal parent (Tarczynski et al. 2003; Martin et al. 2005). with the Lys-containing nonzein proteins (Huang et al. Crosses between the maternal PE5 and the paternal RNAi 2006). Doubling the Lys levels without changing the protein lines were performed during the summer of 2014 and 2015. content in corn could add up to $480 million in annual gross PE5; g- plants generated during the summer of 2014 were value to US corn in the global feed market (Johnson et al. crossed with aRNAi during the summer of 2015. The rest of 2000). the crosses of g/bRNAi, bRNAi, and aRNAi with PE5 were Among the maize opaque kernel mutants that affect the made during the summer of 2014. These crosses gave five accumulation of the zeins, only a few have been reported that distinct ears that were used for analysis: (1) PE5;aRNAi, (2) alter the synthesis of the g-zeins. The maize Mucronate mu- PE5;b-, (3) PE5;g-, (4) PE5;g-/b-, and (5) PE5;g-/a-. tation is a deletion in the 16-kDa g-zein that produces an Genotyping abnormal 16-kDa g-zein, whereas opaque-15 reduces the 27-kDa g-zein synthesis and appears to be a mutation of an Genomic DNA was isolated from maize leaves at the three- to o2 modifier gene (Dannenhoffer et al. 1995; Kim et al. 2006). four-leaf stage using a modified CTAB extraction method Near-isogenic lines of several high-Lys opaque mutants in the (Sawa et al. 1997). For extraction of genomic DNA from W64A genetic background showed that o2 has the highest mature maize kernels, a portion of the kernel that is mostly kernel Lys content among the opaque mutants (Hunter et al. endospermwithnoembryotissuesweregroundtoafine pow- 2002). Efforts to improve the protein quality of maize seeds der and subjected to DNA extraction with the Nucleospin Plant have focused on o2 seeds as other opaque mutants offer no II kit (Takara Bio). Transgenic plants were screened for the additional advantage over o2 in terms of Lys content and presence of both RNAi and EcPAPR transgenes using the primer nutritional quality.
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