Non-syntenic genes drive RTCS-dependent regulation of the embryo transcriptome during formation of seminal root primordia in maize (<i>Zea mays</i>L.)

Tai, Huanhuan; Opitz, Nina; Lithio, Andrew; Lü, Xin; Nettleton, Dan; Hochholdinger, Frank

doi:10.1093/jxb/erw422

Cited by 11 publications

(15 citation statements)

References 59 publications

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“…The high developmental and the low genotypic conservation of SPE patterns is in line with their transcriptomic relationship ( Figure 1B). Similar observations have been made in a comparison of different genotypes of maize during seminal root development [14]. In addition, SPE patterns displayed 75% conservation in maize roots subjected to water deficit treatment versus control conditions [11].…”

Section: Spe Complementation Is Universal In Maize Hybridssupporting

confidence: 80%

Single-Parent Expression Is a General Mechanism Driving Extensive Complementation of Non-syntenic Genes in Maize Hybrids

et al. 2018

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Maize (Zea mays L.) displays an exceptional degree of structural genomic diversity [1, 2]. In addition, variation in gene expression further contributes to the extraordinary phenotypic diversity and plasticity of maize. This study provides a systematic investigation on how distantly related homozygous maize inbred lines affect the transcriptomic plasticity of their highly heterozygous F hybrids. The classical dominance model of heterosis explains the superiority of hybrid plants by the complementation of deleterious parental alleles by superior alleles of the second parent at many loci [3]. Genes active in one inbred line but inactive in another represent an extreme instance of allelic diversity defined as single-parent expression [4]. We observed on average ∼1,000 such genes in all inbred line combinations during primary root development. These genes consistently displayed expression complementation (i.e., activity) in their hybrid progeny. Consequently, extreme expression complementation is a general mechanism that results on average in ∼600 additionally active genes and their encoded biological functions in hybrids. The modern maize genome is complemented by a set of non-syntenic genes, which emerged after the separation of the maize and sorghum lineages and lack syntenic orthologs in any other grass species [5]. We demonstrated that non-syntenic genes are the driving force of gene expression complementation in hybrids. Among those, the highly diversified families of bZIP and bHLH transcription factors [6] are systematically overrepresented. In summary, extreme gene expression complementation extensively shapes the transcriptomic plasticity of maize hybrids and might therefore be one factor controlling the developmental plasticity of hybrids.

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Section: Spe Complementation Is Universal In Maize Hybridssupporting

confidence: 80%

Single-Parent Expression Is a General Mechanism Driving Extensive Complementation of Non-syntenic Genes in Maize Hybrids

et al. 2018

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“…The exact functions of these nonsyntenic genes are largely unknown, because they are underrepresented in classical genetics studies in maize 39 . These nonsyntenic genes may play important roles in some lineage-specific functions, as demonstrated in a study on root development 40 . Evaluating the contribution of these nonsyntenic genes to quantitative phenotypic variations of agronomic traits would be an interesting future pursuit.…”

Section: Discussionmentioning

confidence: 96%

Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes

et al. 2018

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Maize is an important crop with a high level of genome diversity and heterosis. The genome sequence of a typical female line, B73, was previously released. Here, we report a de novo genome assembly of a corresponding male representative line, Mo17. More than 96.4% of the 2,183 Mb assembled genome can be accounted for by 362 scaffolds in ten pseudochromosomes with 38,620 annotated protein-coding genes. Comparative analysis revealed large gene-order and gene structural variations: approximately 10% of the annotated genes were mutually nonsyntenic, and more than 20% of the predicted genes had either large-effect mutations or large structural variations, which might cause considerable protein divergence between the two inbred lines. Our study provides a high-quality reference-genome sequence of an important maize germplasm, and the intraspecific gene order and gene structural variations identified should have implications for heterosis and genome evolution.

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“…In maize, SRN and length were positively correlated with shoot weight under low phosphorous levels (Zhu et al, 2006) and with grain yield under both low and high nitrogen levels (Abdel-Ghani et al, 2015). It has been suggested that SRN has been selected inadvertently as an adaptive trait during domestication (Salvi, 2017;Tai et al, 2017).…”

Section: Selection Pressure Towards Higher Seminal Root Counts Durimentioning

confidence: 99%

Activation of seminal root primordia during wheat domestication reveals underlying mechanisms of plant resilience

Golan

Hendel

Espitia

et al. 2018

Plant Cell & Environment

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Seminal roots constitute the initial wheat root system and provide the main route for water absorption during early stages of development. Seminal root number (SRN) varies among species. However, the mechanisms through which SRN is controlled and in turn contribute to environmental adaptation are poorly understood. Here, we show that SRN increased upon wheat domestication from 3 to 5 due to the activation of 2 root primordia that are suppressed in wild wheat, a trait controlled by loci expressed in the germinating embryo. Suppression of root primordia did not limit water uptake, indicating that 3 seminal roots is adequate to maintain growth during seedling development. The persistence of roots at their primordial state promoted seedling recovery from water stress through reactivation of suppressed primordia upon rehydration. Our findings suggest that under well-watered conditions, SRN is not a limiting factor, and excessive number of roots may be costly and maladaptive. Following water stress, lack of substantial root system suppresses growth and rapid recovery of the root system is essential for seedling recovery. This study underscores SRN as key adaptive trait that was reshaped upon domestication. The maintenance of roots at their primordial state during seedling development may be regarded as seedling protective mechanism against water stress.

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Non-syntenic genes drive RTCS-dependent regulation of the embryo transcriptome during formation of seminal root primordia in maize (Zea maysL.)

Abstract: HighlightRTCS regulates the expression of non-syntenic genes and genes associated with phytohormone action, transcription factors, and cell cycle regulators to control seminal root initiation during embryogenesis in maize.

Cited by 11 publications

References 59 publications

Single-Parent Expression Is a General Mechanism Driving Extensive Complementation of Non-syntenic Genes in Maize Hybrids

Single-Parent Expression Is a General Mechanism Driving Extensive Complementation of Non-syntenic Genes in Maize Hybrids

Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes

Activation of seminal root primordia during wheat domestication reveals underlying mechanisms of plant resilience

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