Transcript profiles in cortical cells of maize primary root during ethylene-induced lysigenous aerenchyma formation under aerobic conditions

Takahashi, Hirokazu; Yamauchi, Takaki; Rajhi, Imene; Nishizawa, Naoko K.; Nakazono, Mikio

doi:10.1093/aob/mcv018

Cited by 53 publications

(45 citation statements)

References 56 publications

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“…6A) in ZmPgb-suppressing roots under hypoxic conditions, supporting the contention that ROS are required for the induction of the death program. ROS are implicated in several PCD-inducing responses in maize, including the formation of aerenchyma in hypoxic roots (Takahashi et al, 2015) and shaping the body of developing somatic embryos (Huang et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Synthesized during adverse growing conditions, ethylene accumulates preferentially in hypoxic tissue, and its production is regulated by the activity of ACS and ACO, encoded by multigene families (Gallie and Young, 2004). A rapid transcriptional induction of several members of ACS and ACO multigene families, as well as the ethylene signalingrelated genes Ebf1 and Erf2, follows exposure to low oxygen (Geisler-Lee et al, 2010;Takahashi et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

“…The ethylene response at the root tip was assessed by measuring the expression of two genes with high homology to EIN3-BINDING F-BOX PROTEIN1 (Ebf1) and ETHYLENE-RESPONSIVE FACTOR2 (Erf2), known mediators of ethylene signaling in maize roots (Takahashi et al, 2015). Relative to the wild type, the expression of both ZmErf2 and ZmEbf1 was induced rapidly in Figure 5.…”

Section: Spatial and Temporal Regulation Of Ethylene Biosynthetic Andmentioning

confidence: 99%

“…DPI is used frequently as an inhibitor of NADPH oxidase, reducing ROS production (Takahashi et al, 2015), although it does inhibit other flavoprotein-containing enzymes (Wind et al, 2010). 1-MCP competes with ethylene, inhibiting its perception, and is thought to be specific in its action (Sisler and Serek, 1997).…”

Section: Ethylene Mediates the Zmpgb Regulation Of Ros Pcd And Growmentioning

confidence: 99%

“…The execution of PCD in maize (Zea mays) roots under hypoxic conditions is triggered by a rapid increase in ethylene level resulting from the transcriptional induction of 1-aminocyclopropane-1-carboxylate synthase (ACS) and oxidase (ACO; Geisler- Lee et al, 2010) and transduced through the generation of reactive oxygen species (ROS) produced by NADPH oxidase activity (Torres and Dangl, 2005). The progression of these events in maize roots has been shown using 1-methylcyclopropene (1-MCP) as a specific inhibitor of ethylene perception or diphenyleneiodonium (DPI) to inhibit ROS production (Takahashi et al, 2015).…”

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confidence: 99%

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Phytoglobins Improve Hypoxic Root Growth by Alleviating Apical Meristem Cell Death

2016

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Hypoxic root growth in maize (Zea mays) is influenced by the expression of phytoglobins (ZmPgbs). Relative to the wild type, suppression of ZmPgb1.1 or ZmPgb1.2 inhibits the growth of roots exposed to 4% oxygen, causing structural abnormalities in the root apical meristems. These effects were accompanied by increasing levels of reactive oxygen species (ROS), possibly through the transcriptional induction of four Respiratory Burst Oxidase Homologs. TUNEL-positive nuclei in meristematic cells indicated the involvement of programmed cell death (PCD) in the process. These cells also accumulated nitric oxide and stained heavily for ethylene biosynthetic transcripts. A sharp increase in the expression level of several 1-aminocyclopropane synthase (ZmAcs2, ZmAcs6, and ZmAcs7), 1-aminocyclopropane oxidase (Aco15, Aco20, Aco31, and Aco35), and ethylene-responsive (ZmErf2 and ZmEbf1) genes was observed in hypoxic ZmPgb-suppressing roots, which overproduced ethylene. Inhibiting ROS synthesis with diphenyleneiodonium or ethylene perception with 1-methylcyclopropene suppressed PCD, increased BAX inhibitor-1, an effective attenuator of the death programs in eukaryotes, and restored root growth. Hypoxic roots overexpressing ZmPgbs had the lowest level of ethylene and showed a reduction in ROS staining and TUNEL-positive nuclei in the meristematic cells. These roots retained functional meristems and exhibited the highest growth performance when subjected to hypoxic conditions. Collectively, these results suggest a novel function of Pgbs in protecting root apical meristems from hypoxiainduced PCD through mechanisms initiated by nitric oxide and mediated by ethylene via ROS.Oxygen deficiency (hypoxia), experienced by plants grown in poorly drained soils or subjected to flooding, impairs plant growth and results in heavy crop losses (Dennis et al., 2000). Submergence or flooding reduces oxygen availability for plant cells, inhibiting the gas exchange required for basic physiological processes (Bailey-Serres and Voesenek, 2008). Both roots and shoots are affected by hypoxia, regardless of whether the plant is submerged or only the root is exposed to the condition. The consequences to shoots of prolonged root hypoxia include reduced photosynthetic rate and stomatal conductance, decreased leaf growth and senescence, wilting of the aboveground organs, and alterations in plant water relations (Mustroph and Albrecht, 2003). Ethylene accumulates rapidly in flooded Rumex palustris root cells (Visser et al., 1996), and in some species, ethylene affects the selective death of cortical cells generating lysogenous aerenchyma (Drew et al., 1979(Drew et al., , 2000; Drew, 1997) Precursors of ethylene have been shown to induce changes in Brassica napus growth behavior and root architecture (Patrick et al., 2009). Depending upon the concentration and species, ethylene can either stimulate or inhibit root growth (Konings and Jackson, 1979). Ethylene regulation of programmed cell death (PCD) is not restricted to hypoxia but, rather, is observed in ...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Spatial and Temporal Regulation Of Ethylene Biosynthetic Andmentioning

confidence: 99%

Section: Ethylene Mediates the Zmpgb Regulation Of Ros Pcd And Growmentioning

confidence: 99%

mentioning

confidence: 99%

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Phytoglobins Improve Hypoxic Root Growth by Alleviating Apical Meristem Cell Death

2016

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Newly identified miRNAs may contribute to aerenchyma formation in sugarcane roots

et al. 2020

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Small RNAs comprise three families of noncoding regulatory RNAs that control gene expression by blocking mRNA translation or leading to mRNA cleavage. Such post‐transcriptional negative regulation is relevant for both plant development and environmental adaptations. An important biotechnological application of miRNA identification is the discovery of regulators and effectors of cell wall degradation, which can improve/facilitate hydrolysis of cell wall polymers for second‐generation bioethanol production. The recent characterization of plant innate cell wall modifications occurring during root aerenchyma development triggered by ethylene led to the possibility of prospection for mechanisms of cell wall disassembly in sugarcane. By using next‐generation sequencing, 39 miRNAs were identified in root segments along the process of aerenchyma development. Among them, 31 miRNAs were unknown to the sugarcane miRBase repository but previously identified as produced by its relative Sorghum bicolor. Key putative targets related to signal transduction, carbohydrate metabolic process, and cell wall organization or biogenesis were among the most representative gene categories targeted by miRNA. They belong to the subclasses of genes associated with the four modules of cell wall modification in sugarcane roots: cell expansion, cell separation, hemicellulose, and cellulose hydrolysis. Thirteen miRNAs possibly related to ethylene perception and signaling were also identified. Our findings suggest that miRNAs may be involved in the regulation of cell wall degradation during aerenchyma formation. This work also points out to potential molecular tools for sugarcane improvement in the context of second‐generation biofuels.

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Sorghum stem aerenchyma formation is regulated by SbNAC_D during internode development

Casto

McKinley

et al. 2018

Plant Direct

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Sorghum bicolor is a drought‐resilient C4 grass used for production of grain, forage, sugar, and biomass. Sorghum genotypes capable of accumulating high levels of stem sucrose have solid stems that contain low levels of aerenchyma. The D ‐locus on SBI 06 modulates the extent of aerenchyma formation in sorghum stems and leaf midribs. A QTL aligned with this locus was identified and fine‐mapped in populations derived from BT x623* IS 320c, BT x623*R07007, and BT x623*Standard broomcorn. Analysis of coding polymorphisms in the fine‐mapped D ‐locus showed that genotypes that accumulate low levels of aerenchyma encode a truncated NAC transcription factor (Sobic.006G147400, SbNAC_d1 ), whereas parental lines that accumulate higher levels of stem aerenchyma encode full‐length NAC TF s ( SbNAC‐D ). During vegetative stem development, aerenchyma levels are low in nonelongated stem internodes, internode growing zones, and nodes. Aerenchyma levels increase in recently elongated internodes starting at the top of the internode near the center of the stem. SbNAC_D was expressed at low levels in nonelongated internodes and internode growing zones and at higher levels in regions of stem internodes that form aerenchyma. SbXCP1 , a gene encoding a cysteine protease involved in programmed cell death, was induced in SbNAC_D genotypes in parallel with aerenchyma formation in sorghum stems but not in SbNAC_d1 genotypes. Several sweet sorghum genotypes encode the recessive SbNAC_d1 allele and have low levels of stem aerenchyma. Based on these results, we propose that SbNAC_D is the D ‐gene identified by Hilton (1916) and that allelic variation in SbNAC_D modulates the extent of aerenchyma formation in sorghum stems.

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Transcript profiles in cortical cells of maize primary root during ethylene-induced lysigenous aerenchyma formation under aerobic conditions

Cited by 53 publications

References 56 publications

Phytoglobins Improve Hypoxic Root Growth by Alleviating Apical Meristem Cell Death

Phytoglobins Improve Hypoxic Root Growth by Alleviating Apical Meristem Cell Death

Newly identified miRNAs may contribute to aerenchyma formation in sugarcane roots

Sorghum stem aerenchyma formation is regulated by SbNAC_D during internode development

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