Maize ARGOS1 (ZAR1) transgenic alleles increase hybrid maize yield

Guo, Mei; Rupe, Mary A.; Wei, Jun; Winkler, Christopher; Goncalves-Butruille, Marymar; Weers, Ben; Cerwick, Sharon; Dieter, Jo Ann; Duncan, Keith E; Howard, Richard J.; Hou, Zhenglin; Löffler, C.; Cooper, Mark; Simmons, Carl R.

doi:10.1093/jxb/ert370

Cited by 105 publications

(91 citation statements)

References 40 publications

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“…Leaf heterosis in maize occurs through increased cell numbers linked with changes in auxin response (55,56). Altered auxin responses are also observed in rice hybrids (57).…”

Section: Discussionmentioning

confidence: 99%

“…Although changes in auxin response are common, the molecular triggers appear to differ between hybrid systems. Micro-RNAs and other small RNAs are linked with changes to the IAA network in hybrid rice (57), whereas in maize hybrids, allele variants of the auxin-regulated transcription factor ZmARGOS1 are contributors (55). In the Arabidopsis hybrids, the increased auxin response mainly involves changes at the level of auxin biosynthesis involving repression of genes involved in producing the defense compounds, indole glucosinolates, and camalexin.…”

Section: Discussionmentioning

confidence: 99%

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Hormone-regulated defense and stress response networks contribute to heterosis inArabidopsisF1 hybrids

Groszmann

González-Bayón

Lyons

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

118

115

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Plant hybrids are extensively used in agriculture to deliver increases in yields, yet the molecular basis of their superior performance (heterosis) is not well understood. Our transcriptome analysis of a number of Arabidopsis F1 hybrids identified changes to defense and stress response gene expression consistent with a reduction in basal defense levels. Given the reported antagonism between plant immunity and growth, we suggest that these altered patterns of expression contribute to the greater growth of the hybrids. The altered patterns of expression in the hybrids indicate decreases to the salicylic acid (SA) biosynthesis pathway and increases in the auxin [indole-3-acetic acid (IAA)] biosynthesis pathway. SA and IAA are hormones known to control stress and defense responses as well as plant growth. We found that IAA-targeted gene activity is frequently increased in hybrids, correlating with a common heterotic phenotype of greater leaf cell numbers. Reduced SA concentration and target gene responses occur in the larger hybrids and promote increased leaf cell size. We demonstrated the importance of SA action to the hybrid phenotype by manipulating endogenous SA concentrations. Increasing SA diminished heterosis in SA-reduced hybrids, whereas decreasing SA promoted growth in some hybrids and phenocopied aspects of hybrid vigor in parental lines. Pseudomonas syringae infection of hybrids demonstrated that the reductions in basal defense gene activity in these hybrids does not necessarily compromise their ability to mount a defense response comparable to the parents.

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“…Leaf heterosis in maize occurs through increased cell numbers linked with changes in auxin response (55,56). Altered auxin responses are also observed in rice hybrids (57).…”

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Hormone-regulated defense and stress response networks contribute to heterosis inArabidopsisF1 hybrids

Groszmann

González-Bayón

Lyons

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

118

115

View full text Add to dashboard Cite

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“…A number of studies have identified overdominant QTL associated with hybrid vigor (23,24,78,81,83,84), but molecular identification of casual variants is rare. Although a few cases of truly overdominant loci have been confirmed (10)(11)(12)(13), in some cases, fine mapping of overdominant QTL has separated a single overdominant locus into multiple, dominant loci acting in repulsion (85,86), a situation called pseudooverdominance, which represents the third common hypothesis for heterosis.…”

Section: Arabidopsis Thaliana In the Context Of Traditional Heterosismentioning

confidence: 99%

“…Three nonmutually exclusive types of intralocus interactions are commonly invoked to explain heterosis. The overdominance hypothesis postulates that a single mutation in the heterozygous state is causal (3,4,9), and it accounts for at least a few cases of heterosis (10)(11)(12)(13) and hybrid inferiority (14,15). The dominance hypothesis suggests that genome-wide complementation of many small-effect, weakly deleterious loci drives hybrid superiority (16)(17)(18), but the small effect size of individual loci would make it difficult, if not impossible, to generate direct support for this hypothesis.…”

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confidence: 99%

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seymour

Chae

Grimm

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The ubiquity of nonparental hybrid phenotypes, such as hybrid vigor and hybrid inferiority, has interested biologists for over a century and is of considerable agricultural importance. Although examples of both phenomena have been subject to intense investigation, no general model for the molecular basis of nonadditive genetic variance has emerged, and prediction of hybrid phenotypes from parental information continues to be a challenge. Here we explore the genetics of hybrid phenotype in 435 Arabidopsis thaliana individuals derived from intercrosses of 30 parents in a half diallel mating scheme. We find that nonadditive genetic effects are a major component of genetic variation in this population and that the genetic basis of hybrid phenotype can be mapped using genome-wide association (GWA) techniques. Significant loci together can explain as much as 20% of phenotypic variation in the surveyed population and include examples that have both classical dominant and overdominant effects. One candidate region inherited dominantly in the half diallel contains the gene for the MADS-box transcription factor AGAMOUS-LIKE 50 (AGL50), which we show directly to alter flowering time in the predicted manner. Our study not only illustrates the promise of GWA approaches to dissect the genetic architecture underpinning hybrid performance but also demonstrates the contribution of classical dominance to genetic variance.T he often observed phenotypic superiority of progeny relative to their parents, or heterosis, is a universal phenomenon and of great importance to plant agriculture. The earliest description of heterosis (also known as hybrid vigor or superiority) dates to Darwin's studies of cross-fertilization in plants. He noticed that intercrossing distantly related individuals gave rise to larger, more vigorous progeny (1). Four decades later, George Shull coined the term "heterosis" (2) for this phenomenon, which he and Edward East had independently described for hybrids of inbred maize in 1908 (3, 4). Heterosis has long been of interest to evolutionary biologists as a potential explanation for the ubiquity of cross-fertilization in plants and animals, but it is also a central component of agricultural breeding programs. The combination of hybrid seed technology and inbred line improvement has driven an unprecedented improvement in maize yield over the past century (5). Despite the economic importance of heterosis and its intensive investigation in a wide spectrum of species, prediction of hybrid performance from parental information remains a major challenge (6).In the terms of quantitative genetics, hybrid vigor (and its opposite, inferiority) describes a deviation of progeny from the phenotypic mean of the parents. This means that heterosis cannot be explained by the addition of the effects of contributing alleles (7). Nonadditive genetic variance can result from a nonlinear phenotypic effect of alleles at one locus, as in the case of dominant/recessive allele pairs in classical genetics, or from epistatic interactions ...

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“…ZmARGOS8 is a member of the AUXIN-REGULATED GENE INVOLVED IN ORGAN SIZE (ARGOS) gene family (Hu et al, 2003), which encode integral membrane proteins localized to the endoplasmic reticulum (ER) and Golgi (Rai et al, 2015;Shi et al, 2015). Arabidopsis ARGOS and homologs from other species promote cell division and/or expansion when overexpressed, affecting organ size in transgenic plants (Hu et al, 2003(Hu et al, , 2006Wang et al, 2009;Kuluev et al, 2011;Feng et al, 2011;Guo et al, 2014). Initially, it was hypothesized that ARGOS may transduce auxin signals downstream of AUXIN RESISTANCE1 to regulate cell proliferation and organ growth through AINTEGUMENTA (Hu et al, 2003).…”

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confidence: 99%

Maize and Arabidopsis ARGOS Proteins Interact with Ethylene Receptor Signaling Complex, Supporting a Regulatory Role for ARGOS in Ethylene Signal Transduction

et al. 2016

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The phytohormone ethylene regulates plant growth and development as well as plant response to environmental cues. ARGOS genes reduce plant sensitivity to ethylene when overexpressed in transgenic Arabidopsis (Arabidopsis thaliana) and maize (Zea mays). A previous genetic study suggested that the endoplasmic reticulum and Golgi-localized maize ARGOS1 targets the ethylene signal transduction components at or upstream of CONSTITUTIVE TRIPLE RESPONSE1, but the mechanism of ARGOS modulating ethylene signaling is unknown. Here, we demonstrate in Arabidopsis that ZmARGOS1, as well as the Arabidopsis ARGOS homolog ORGAN SIZE RELATED1, physically interacts with Arabidopsis REVERSION-TO-ETHYLENE SENSITIVITY1 (RTE1), an ethylene receptor interacting protein that regulates the activity of ETHYLENE RESPONSE1. The protein-protein interaction was also detected with the yeast split-ubiquitin two-hybrid system. Using the same yeast assay, we found that maize RTE1 homolog REVERSION-TO-ETHYLENE SENSITIVITY1 LIKE4 (ZmRTL4) and ZmRTL2 also interact with maize and Arabidopsis ARGOS proteins. Like AtRTE1 in Arabidopsis, ZmRTL4 and ZmRTL2 reduce ethylene responses when overexpressed in maize, indicating a similar mechanism for ARGOS regulating ethylene signaling in maize. A polypeptide fragment derived from ZmARGOS8, consisting of a Pro-rich motif flanked by two transmembrane helices that are conserved among members of the ARGOS family, can interact with AtRTE1 and maize RTL proteins in Arabidopsis. The conserved domain is necessary and sufficient to reduce ethylene sensitivity in Arabidopsis and maize. Overall, these results suggest a physical association between ARGOS and the ethylene receptor signaling complex via AtRTE1 and maize RTL proteins, supporting a role for ARGOS in regulating ethylene perception and the early steps of signal transduction in Arabidopsis and maize.

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Maize ARGOS1 (ZAR1) transgenic alleles increase hybrid maize yield

Cited by 105 publications

References 40 publications

Hormone-regulated defense and stress response networks contribute to heterosis inArabidopsisF1 hybrids

Hormone-regulated defense and stress response networks contribute to heterosis inArabidopsisF1 hybrids

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Maize and Arabidopsis ARGOS Proteins Interact with Ethylene Receptor Signaling Complex, Supporting a Regulatory Role for ARGOS in Ethylene Signal Transduction

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