OPAQUE11 Is a Central Hub of the Regulatory Network for Maize Endosperm Development and Nutrient Metabolism

Feng, Fan; Qi, Weiwei; Lv, Yuanda; Yan, Shumei; Xu, Liming; Yang, Wei; Yuan, Yue; Chen, Yihan; Zhao, Han; Song, Rentao

doi:10.1105/tpc.17.00616

Cited by 100 publications

(102 citation statements)

References 80 publications

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“…Absence of ZmNAC124 expression in the AS was consistent with the strong and specific in situ hybridisation signal for this gene in the basal part of the embryonic axis (Zimmermann and Werr, 2005). The two endosperm-specific genes ZmZOU/O11 (Zm00001d003677) and O2 were found to be strongly expressed in the End and EAS, and weakly in the SAL samples ( Figure 2C) (Feng et al, 2018;Grimault et al, 2015;Schmidt et al, 1990). A weak expression in the Per sample was unexpected but consistent with other transcriptomics data (Sekhon et al, 2011), which could also reflect possible contamination of the Per samples by aleurone layer, since the aleurone layer has a tendency to stick to the pericarp (See discussion part).…”

Section: Rna-seq Profiling Of 13 Dap Maize Kernel Compartments and Emsupporting

confidence: 77%

Transcriptomics at maize embryo/endosperm interfaces identify a novel transcriptionally distinct endosperm sub-domain adjacent to the embryo scutellum (EAS)

Doll

Just

Brunaud

et al. 2019

Preprint

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Seeds are complex biological systems comprising three genetically distinct tissues nested one inside another (embryo, endosperm and maternal tissues). However, the complexity of the kernel makes it difficult to understand inter compartment interactions without access to spatially accurate information. Here we took advantage of the large size of the maize kernel to characterize genome-wide expression profiles of tissues at embryo/endosperm interfaces.Our analysis identifies specific transcriptomic signatures in two interface tissues compared to whole seed compartments: The scutellar aleurone layer (SAL), and the newly named endosperm adjacent to scutellum (EAS). The EAS, which appears around 9 days after pollination and persists for around 11 days, is confined to one to three endosperm cell layers adjacent to the embryonic scutellum. Its transcriptome is enriched in genes encoding transporters. The absence of the embryo in an embryo specific (emb) mutant can alter the expression pattern of EAS marker genes. The detection of cell death in some EAS cells together with an accumulation of crushed cell walls suggests that the EAS is a dynamic zone from which cell layers in contact with the embryo are regularly eliminated, and to which additional endosperm cells are recruited as the embryo grows.

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Section: Rna-seq Profiling Of 13 Dap Maize Kernel Compartments and Emsupporting

confidence: 77%

Transcriptomics at maize embryo/endosperm interfaces identify a novel transcriptionally distinct endosperm sub-domain adjacent to the embryo scutellum (EAS)

Doll

Just

Brunaud

et al. 2019

Preprint

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“…It was also highly notable that the opaque‐2 gene ( O2 , GRMZM2G015534), the long‐studied and well‐known regulator of zein gene expression (Zhang et al ., ), was among the 53 targets of this eQTL. Likewise, the basic helix‐loop‐helix (bHLH) gene ZmICE1 (GRMZM2G173534) — which encodes a protein that strongly interacts with O11, a central regulator of endosperm development and nutrient metabolism that directly regulates the expression of O2 on the upstream (Feng et al ., )—was also among the 53 associated genes. Beyond this, ZmICE1 , O2 as well as the 10 zein genes had significantly higher expression levels in the large kernel haplotype (Figure S6).…”

Section: Resultsmentioning

confidence: 94%

Kernel size‐related genes revealed by an integrated eQTL analysis during early maize kernel development

Pang

Zong

et al. 2019

The Plant Journal

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SummaryIn maize, kernel traits strongly impact overall grain yields, and it is known that sophisticated spatiotemporal programs of gene expression coordinate kernel development, so advancing our knowledge of kernel development can help efforts to improve grain yields. Here, using phenotype, genotype and transcriptomics data of maize kernels at 5 and 15 days after pollination (DAP) for a large association mapping panel, we employed multiple quantitative genetics approaches—genome‐wide association studies (GWAS) as well as expression quantitative trait loci (eQTL) and quantitative trait transcript (QTT) analyses—to gain insights about molecular genetic basis of kernel development in maize. This resulted in the identification of 137 putative kernel length‐related genes at 5 DAP, of which 43 are located in previously reported QTL regions. Strikingly, we identified an eQTL that overlaps the locus encoding a maize homolog of the recently described m6A methylation reader protein ECT2 from Arabidopsis; this putative epieQTL is associated with 53 genes and may represent a master epi‐transcriptomic regulator of kernel development. Notably, among the genes associated with this epieQTL, 10 are for the main storage proteins in the maize endosperm (zeins) and two are known regulators of zein expression or endosperm development (Opaque2 and ZmICE1). Collectively, beyond cataloging and characterizing genomic attributes of a large number of eQTL associated with kernel development in maize, our study highlights how an eQTL approach can bolster the impact of both GWAS and QTT studies and can drive insights about the basic biology of plants.

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“…As easily detectable phenotypes, mutants with opaque or floury endosperm have been identified, characterized and functionally elucidated. Generally, these mutants have been grouped into several classes, based on their phenotypes: first, mutants with opaque endosperm and decreased seed weight but normal seed size, such as o2 , o7 and nkd (Schmidt et al ; Wang et al ; Yi et al ; Gontarek et al ); second, those with opaque endosperm and decreases in both seed size and seed weight, such as o5 , o11 and floury3 (Myers et al ; Li et al ; Feng et al ); third, those with opaque endosperm and misshapen protein bodies but no alteration of zein or non‐zein protein contents, such as o1 and o10 (Wang et al ; Yao et al ); and fourth, those with opaque endosperm and both misshapen protein bodies and decreased zein content, such as floury2 , Mucronate ( Mc ) and DeB30 (Coleman et al ; Kim et al ; Kim et al ).…”

Section: Discussionmentioning

confidence: 99%

“…So far, many genes corresponding to opaque and floury endosperm have been shown to encode enzymes involved in zein protein and starch synthesis (for example, Kim et al 2004;Holding et al 2007;Miclaus et al 2011;Myers et al 2011;Wang et al 2011;Wang et al 2012;Yao et al 2016). But only a few regulators of endosperm development have been cloned and www.jipb.net XXX 2019 | Volume XXXX | Issue XXXX | XXX-XX functionally investigated: O2, O11 and floury 3 (Schmidt et al 1990;Li et al 2017;Feng et al 2018).…”

Section: Os1 Might Be a Master Regulator In Maizementioning

confidence: 99%

OS1 functions in the allocation of nutrients between the endosperm and embryo in maize seeds

Song

Zhu

Zhao

et al. 2019

JIPB

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Uncovering the genetic basis of seed development will provide useful tools for improving both crop yield and nutritional value. However, the genetic regulatory networks of maize (Zea mays) seed development remain largely unknown. The maize opaque endosperm and small germ 1 (os1) mutant has opaque endosperm and a small embryo. Here, we cloned OS1 and show that it encodes a putative transcription factor containing an RWP‐RK domain. Transcriptional analysis indicated that OS1 expression is elevated in early endosperm development, especially in the basal endosperm transfer layer (BETL), conducting zone (CZ), and central starch endosperm (CSE) cells. RNA sequencing (RNA‐Seq) analysis of the os1 mutant revealed sharp downregulation of certain genes in specific cell types, including ZmMRP‐1 and Meg1 in BETL cells and a majority of zein‐ and starch‐related genes in CSE cells. Using a haploid induction system, we show that wild‐type endosperm could rescue the smaller size of os1 embryo, which suggests that nutrients are allocated by the wild‐type endosperm. Therefore, our data imply that the network regulated by OS1 accomplishes a key step in nutrient allocation between endosperm and embryo within maize seeds. Identification of this network will help uncover the mechanisms regulating the nutritional balance between endosperm and embryo.

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OPAQUE11 Is a Central Hub of the Regulatory Network for Maize Endosperm Development and Nutrient Metabolism

Cited by 100 publications

References 80 publications

Transcriptomics at maize embryo/endosperm interfaces identify a novel transcriptionally distinct endosperm sub-domain adjacent to the embryo scutellum (EAS)

Transcriptomics at maize embryo/endosperm interfaces identify a novel transcriptionally distinct endosperm sub-domain adjacent to the embryo scutellum (EAS)

Kernel size‐related genes revealed by an integrated eQTL analysis during early maize kernel development

OS1 functions in the allocation of nutrients between the endosperm and embryo in maize seeds

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