scispace - formally typeset
Search or ask a question
Journal Article•DOI•

Constitutive Expression of a miR319 Gene Alters Plant Development and Enhances Salt and Drought Tolerance in Transgenic Creeping Bentgrass

Man Zhou1, Dayong Li1, Zhigang Li1, Qian Hu1, Yang Chunhua2, Lihuang Zhu2, Hong Luo1 •
Clemson University1, Chinese Academy of Sciences2
01 Mar 2013-Plant Physiology (American Society of Plant Biologists)-Vol. 161, Iss: 3, pp 1375-1391
TL;DR: The enhanced abiotic stress tolerance in transgenic plants is related to significant down-regulation of miR319 target genes, implying their potential for use in the development of novel molecular strategies to genetically engineer crop species for enhanced resistance to environmental stress.
Abstract: MicroRNA319 (miR319) is one of the first characterized and conserved microRNA families in plants and has been demonstrated to target TCP (for TEOSINTE BRANCHED/CYCLOIDEA/PROLIFERATING CELL FACTORS [PCF]) genes encoding plant-specific transcription factors. MiR319 expression is regulated by environmental stimuli, suggesting its involvement in plant stress response, although experimental evidence is lacking and the underlying mechanism remains elusive. This study investigates the role that miR319 plays in the plant response to abiotic stress using transgenic creeping bentgrass (Agrostis stolonifera) overexpressing a rice (Oryza sativa) miR319 gene, Osa-miR319a. We found that transgenic plants overexpressing Osa-miR319a displayed morphological changes and exhibited enhanced drought and salt tolerance associated with increased leaf wax content and water retention but reduced sodium uptake. Gene expression analysis indicated that at least four putative miR319 target genes, AsPCF5, AsPCF6, AsPCF8, and AsTCP14, and a homolog of the rice NAC domain gene AsNAC60 were down-regulated in transgenic plants. Our results demonstrate that miR319 controls plant responses to drought and salinity stress. The enhanced abiotic stress tolerance in transgenic plants is related to significant down-regulation of miR319 target genes, implying their potential for use in the development of novel molecular strategies to genetically engineer crop species for enhanced resistance to environmental stress.

Content maybe subject to copyright    Report

Citations
More filters
Journal Article•DOI•
Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants

[...]

Mohammed Nuruzzaman1, Akhter Most Sharoni, Shoshi Kikuchi•
Saitama University1
03 Sep 2013-Frontiers in Microbiology
TL;DR: An overview of the regulation of the stress responsive NAC SNAC/(IX) group of genes that are implicated in the resistance to different stresses is presented and it is reviewed that their overexpression can improve stress tolerance via biotechnological approaches.
Abstract: NAC transcription factors are one of the largest families of transcriptional regulators in plants, and members of the NAC gene family have been suggested to play important roles in the regulation of the transcriptional reprogramming associated with plant stress responses. A phylogenetic analysis of NAC genes, with a focus on rice and Arabidopsis, was performed. Herein, we present an overview of the regulation of the stress responsive NAC SNAC/(IX) group of genes that are implicated in the resistance to different stresses. SNAC factors have important roles for the control of biotic and abiotic stresses tolerance and that their overexpression can improve stress tolerance via biotechnological approaches. We also review the recent progress in elucidating the roles of NAC transcription factors in plant biotic and abiotic stresses. Modification of the expression pattern of transcription factor genes and/or changes in their activity contribute to the elaboration of various signaling pathways and regulatory networks. However, a single NAC gene often responds to several stress factors, and their protein products may participate in the regulation of several seemingly disparate processes as negative or positive regulators. Additionally, the NAC proteins function via auto-regulation or cross-regulation is extensively found among NAC genes. These observations assist in the understanding of the complex mechanisms of signaling and transcriptional reprogramming controlled by NAC proteins.

603 citations

Cites background from "Constitutive Expression of a miR319..."

  • ...Transcription S. italica Puranik et al., 2011 ANAC102 Waterlogging Overexpression A. thaliana Christianson et al., 2009 HSImyb and HSINAC Gibberellin response Transcript H. vulgare Robertson, 2004 ANAC042 it is also in biotic Heat stress Overexpression A. thaliana ShahnejatBushehri et al., 2012 TaNAC2a, TaNAC4a, TaNAC6, TaNAC7, TaNAC13 and TaNTL5 Dehydration, salinity and low temperature Transgenic T. aestivum Tang et al., 2012 TaNAC4 Environmental stimuli, including high salinity, wounding, and low-temperature also induced Transcription T. aestivum Xia et al., 2010a ONAC063 High-temperature and high-salinity Transactivation O. sativa Yokotani et al., 2009 www.frontiersin.org September 2013 | Volume 4 | Article 248 | 9 et al., 2012), TaNAC69 (Xue et al., 2011), CarNAC3 (Peng et al., 2009), miR319, AsNAC60 (Zhou et al., 2013), AhNAC2 (Liu et al., 2011), RhNAC2 or RhEXPA4 (Dai et al., 2012), ClNAC (Huang et al., 2012), CsNAM (Paul et al., 2012), SiNAC (Puranik et al., 2011), HSImyb and HSINAC (Robertson, 2004), and TaNAC2a, TaNAC4a, TaNAC6, and TaNAC4 (Tang et al., 2012; Xia et al., 2010a), were increased by drought and NaCl (Figure 5; Table 2)....

    [...]

  • ...…drought, ethephon, ABA, IAA signaling Transcriptome C. arietinum Peng et al., 2009 miR319, AsNAC60 Drought and salinity stress Agrostis stolonifera Zhou et al., 2013 EcNAC1 Water-deficit and salt stress Overexpression N. tabacum Ramegowda et al., 2012 AhNAC2 Salt Overexpression Arachis Liu et…...

    [...]

  • ...Os03g12120, Os03g59730, Os06g15690, Os08g06140, Os08g33670 Panicle, severe drought Microarray O. sativa Nuruzzaman et al., 2012b Os12g41680, Os07g48550, Os11g03300, Os12g03040, Os01g66120, Os05g34830, Cold, drought, submergence, laidown-submergnece Microarray O. sativa Nuruzzaman et al., 2010 Os02g34970, Os07g48450, Os01g01430, Os01g48460 Drought, submergence, laidown-submergnece Microarray O. sativa Nuruzzaman et al., 2010 OsOAT, SNAC2 Drought and oxidative stress tolerance Overexpression O. sativa You et al., 2013 SNAC1, OsSRO1c Oxidative stress tolerance Overexpression O. sativa You et al., 2013 TaNAC69 PEG-induced dehydration Overexpression T. aestivum Xue et al., 2011 GmNAC11, DREB1A, ERD11, Cor15A, ERF5, RAB18, KAT2 Salt tolerance in soybean transgenic hairy roots Overexpression G. max Hao et al., 2011 GmNAC glycoside hydrolases, defensins and glyoxalase I family proteins Drought stress Soybean array GeneChip G. max Le et al., 2011 GmNAC085 Dehydration stress Soybean Affymetrix array G. max Le et al., 2011 TaNAC2a Drought tolerance Overexpression N. tabacum Tang et al., 2012 DgNAC1 ABA, NaCl, drought and cold Overexpression N. tabacum Liu et al., 2011 CarNAC3 Seed germination, drought, ethephon, ABA, IAA signaling Transcriptome C. arietinum Peng et al., 2009 miR319, AsNAC60 Drought and salinity stress Agrostis stolonifera Zhou et al., 2013 EcNAC1 Water-deficit and salt stress Overexpression N. tabacum Ramegowda et al., 2012 AhNAC2 Salt Overexpression Arachis Liu et al., 2011 RhNAC2 or RhEXPA4 Dehydration tolerance Transgenic R. hybrida Dai et al., 2012 ClNAC Hormonal treatments including salt, drought, cold, heat, abscisic acid and salicylic acid treatments Reverse transcriptase polymerase chain reaction C. lavandulifolium Huang et al., 2012 CsNAM Drought, osmoticum, salt, heat and hydrogen peroxide Camellia sinensis Paul et al., 2012 Os04g0477300 Boron-toxicity tolerance RNA interference O. sativa Ochiai et al., 2011 SiNAC Dehydration, salinity, ethephon, and methyl jasmonate....

    [...]

  • ...…September 2013 | Volume 4 | Article 248 | 9 et al., 2012), TaNAC69 (Xue et al., 2011), CarNAC3 (Peng et al., 2009), miR319, AsNAC60 (Zhou et al., 2013), AhNAC2 (Liu et al., 2011), RhNAC2 or RhEXPA4 (Dai et al., 2012), ClNAC (Huang et al., 2012), CsNAM (Paul et al., 2012), SiNAC…...

    [...]

Journal Article•DOI•
Abiotic stress responses in plants.

[...]

Huiming Zhang1, Jianhua Zhu2, Zhizhong Gong3, Zhizhong Gong4, Jian-Kang Zhu1 •
Chinese Academy of Sciences1, University of Maryland, College Park2, Hebei University3, University of Minnesota4
24 Sep 2021-Nature Reviews Genetics
TL;DR: In this paper, the molecular mechanisms underlying the responses of plants to abiotic stresses emphasizes their multilevel nature; multiple processes are involved, including sensing, signalling, transcription, transcript processing, translation and post-translational protein modifications.
Abstract: Plants cannot move, so they must endure abiotic stresses such as drought, salinity and extreme temperatures. These stressors greatly limit the distribution of plants, alter their growth and development, and reduce crop productivity. Recent progress in our understanding of the molecular mechanisms underlying the responses of plants to abiotic stresses emphasizes their multilevel nature; multiple processes are involved, including sensing, signalling, transcription, transcript processing, translation and post-translational protein modifications. This improved knowledge can be used to boost crop productivity and agricultural sustainability through genetic, chemical and microbial approaches.

397 citations

Journal Article•DOI•
MicroRNA: a new target for improving plant tolerance to abiotic stress

[...]

Baohong Zhang1•
East Carolina University1
01 Apr 2015-Journal of Experimental Botany
TL;DR: More function and expression studies will be necessary in order to elucidate the common miRNA-mediated regulatory mechanisms that underlie tolerance to different abiotic stresses, and the use of artificial miRNAs, as well as overexpression and knockout/down of both mi RNAs and their targets, will be the best techniques for determining the specific roles of individual miRNAAs in response to environmental stresses.
Abstract: MicroRNAs (miRNAs) are an extensive class of endogenous, small RNA molecules that sit at the heart of regulating gene expression in multiple developmental and signalling pathways. Recent studies have shown that abiotic stresses induce aberrant expression of many miRNAs, thus suggesting that miRNAs may be a new target for genetically improving plant tolerance to certain stresses. These studies have also shown that miRNAs respond to environmental stresses in a miRNA-, stress-, tissue-, and genotype-dependent manner. During abiotic stress, miRNAs function by regulating target genes within the miRNA-target gene network and by controlling signalling pathways and root development. Generally speaking, stress-induced miRNAs lead to down-regulation of negative regulators of stress tolerance whereas stress-inhibited miRNAs allow the accumulation and function of positive regulators. Currently, the majority of miRNA-based studies have focused on the identification of miRNAs that are responsive to different stress conditions and analysing their expression profile changes during these treatments. This has predominately been accomplished using deep sequencing technologies and other expression analyses, such as quantitative real-time PCR. In the future, more function and expression studies will be necessary in order to elucidate the common miRNA-mediated regulatory mechanisms that underlie tolerance to different abiotic stresses. The use of artificial miRNAs, as well as overexpression and knockout/down of both miRNAs and their targets, will be the best techniques for determining the specific roles of individual miRNAs in response to environmental stresses.

392 citations

Cites background from "Constitutive Expression of a miR319..."

  • ...A  transgenic study found that constitutive expression of miR319 in creeping bentgrass significantly enhanced plant tolerance to salinity and drought stress, and also altered plant development (Zhou et  al., 2013)....

    [...]

Journal Article•DOI•
Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.).

[...]

Chunhua Yang1, Dayong Li1, D. Mao1, Xue Liu1, Chengjun Ji2, Xiaobing Li1, Xianfeng Zhao1, Zhukuan Cheng1, Caiyan Chen1, Lihuang Zhu1 •
Chinese Academy of Sciences1, Peking University2
01 Dec 2013-Plant Cell and Environment
TL;DR: It is demonstrated that miR319 plays important roles in leaf morphogenesis and cold tolerance in rice and genetically down-regulating the expression of either of the two miR 319-targeted genes in RNA interference plants resulted in enhanced cold tolerance after chilling acclimation.
Abstract: MicroRNA319 (miR319) family is one of the conserved microRNA (miRNA) families among diverse plant species. It has been reported that miR319 regulates plant development in dicotyledons, but little is known at present about its functions in monocotyledons. In rice (Oryza sativa L.), the MIR319 gene family comprises two members, Osa-MIR319a and Osa-MIR319b. Here, we report an expression pattern analysis and a functional characterization of the two Osa-MIR319 genes in rice. We found that overexpressing Osa-MIR319a and Osa-MIR319b in rice both resulted in wider leaf blades. Leaves of osa-miR319 overexpression transgenic plants showed an increased number of longitudinal small veins, which probably accounted for the increased leaf blade width. In addition, we observed that overexpressing osa-miR319 led to enhanced cold tolerance (4 °C) after chilling acclimation (12 °C) in transgenic rice seedlings. Notably, under both 4 and 12 °C low temperatures, Osa-MIR319a and Osa-MIR319b were down-regulated while the expression of miR319-targeted genes was induced. Furthermore, genetically down-regulating the expression of either of the two miR319-targeted genes, OsPCF5 and OsPCF8, in RNA interference (RNAi) plants also resulted in enhanced cold tolerance after chilling acclimation. Our findings in this study demonstrate that miR319 plays important roles in leaf morphogenesis and cold tolerance in rice.

303 citations

Journal Article•DOI•
MicroRNAs As Potential Targets for Abiotic Stress Tolerance in Plants

[...]

Varsha Shriram1, Vinay Kumar1, Rachayya M. Devarumath, Tushar Khare1, Shabir H. Wani2 •
Savitribai Phule Pune University1, Sher-e-Kashmir University of Agricultural Sciences and Technology2
14 Jun 2016-Frontiers in Plant Science
TL;DR: Recent updates on plant miRNAs, their biogenesis and functions, target prediction and identification, computational tools and databases available, and their roles in abiotic stress-responses and adaptive mechanisms in major crop plants are provided.
Abstract: The microRNAs (miRNAs) are small (20-24 nt) sized, non-coding, single stranded riboregulator RNAs abundant in higher organisms. Recent findings have established that plants assign miRNAs as critical post-transcriptional regulators of gene expression in sequence-specific manner to respond to numerous abiotic stresses they face during their growth cycle. These small RNAs regulate gene expression via translational inhibition. Usually, stress induced miRNAs downregulate their target mRNAs, whereas, their downregulation leads to accumulation and function of positive regulators. In the past decade, investigations were mainly aimed to identify plant miRNAs, responsive to individual or multiple environmental factors, profiling their expression patterns and recognizing their roles in stress responses and tolerance. Altered expressions of miRNAs implicated in plant growth and development have been reported in several plant species subjected to abiotic stress conditions such as drought, salinity, extreme temperatures, nutrient deprivation, and heavy metals. These findings indicate that miRNAs may hold the key as potential targets for genetic manipulations to engineer abiotic stress tolerance in crop plants. This review is aimed to provide recent updates on plant miRNAs, their biogenesis and functions, target prediction and identification, computational tools and databases available for plant miRNAs, and their roles in abiotic stress-responses and adaptive mechanisms in major crop plants. Besides, the recent case studies for overexpressing the selected miRNAs for miRNA-mediated enhanced abiotic stress tolerance of transgenic plants have been discussed.

279 citations

Cites background from "Constitutive Expression of a miR319..."

  • ...Overexpression of osa-miR319a in creeping bentgrass (Agrostis stolonifera) significantly improved the salt and drought tolerance of transgenic plants (Zhou et al., 2013)....

    [...]

References
More filters
Journal Article•DOI•
Mechanisms of salinity tolerance

[...]

Rana Munns, Mark Tester
29 Apr 2008-Annual Review of Plant Biology
TL;DR: The physiological and molecular mechanisms of tolerance to osmotic and ionic components of salinity stress are reviewed at the cellular, organ, and whole-plant level and the role of the HKT gene family in Na(+) exclusion from leaves is increasing.
Abstract: The physiological and molecular mechanisms of tolerance to osmotic and ionic components of salinity stress are reviewed at the cellular, organ, and whole-plant level. Plant growth responds to salinity in two phases: a rapid, osmotic phase that inhibits growth of young leaves, and a slower, ionic phase that accelerates senescence of mature leaves. Plant adaptations to salinity are of three distinct types: osmotic stress tolerance, Na + or Cl − exclusion, and the tolerance of tissue to accumulated Na + or Cl − . Our understanding of the role of the HKT gene family in Na + exclusion from leaves is increasing, as is the understanding of the molecular bases for many other transport processes at the cellular level. However, we have a limited molecular understanding of the overall control of Na + accumulation and of osmotic stress tolerance at the whole-plant level. Molecular genetics and functional genomics provide a new opportunity to synthesize molecular and physiological knowledge to improve the salinity tolerance of plants relevant to food production and environmental sustainability.

9,966 citations

"Constitutive Expression of a miR319..." refers background in this paper

  • ...At the physiological level, plant responses to salinity stress are generally divided into two phases: a rapid, osmotic phase inhibiting shoot growth and a slower, ionic phase accelerating the senescence of mature leaves (Munns and Tester, 2008)....

    [...]

Journal Article•DOI•
Comparative physiology of salt and water stress

[...]

Rana Munns1•
Commonwealth Scientific and Industrial Research Organisation1
01 Feb 2002-Plant Cell and Environment
TL;DR: It is important to avoid treatments that induce cell plasmolysis, and to design experiments that distinguish between tolerance of salt and tolerance of water stress, to understand the processes that give rise toolerance of salt, as distinct from tolerance of osmotic stress.
Abstract: Plant responses to salt and water stress have much in common. Salinity reduces the ability of plants to take up water, and this quickly causes reductions in growth rate, along with a suite of metabolic changes identical to those caused by water stress. The initial reduction in shoot growth is probably due to hormonal signals generated by the roots. There may be salt-specific effects that later have an impact on growth; if excessive amounts of salt enter the plant, salt will eventually rise to toxic levels in the older transpiring leaves, causing premature senescence, and reduce the photosynthetic leaf area of the plant to a level that cannot sustain growth. These effects take time to develop. Salttolerant plants differ from salt-sensitive ones in having a low rate of Na + and Cl ‐ transport to leaves, and the ability to compartmentalize these ions in vacuoles to prevent their build-up in cytoplasm or cell walls and thus avoid salt toxicity. In order to understand the processes that give rise to tolerance of salt, as distinct from tolerance of osmotic stress, and to identify genes that control the transport of salt across membranes, it is important to avoid treatments that induce cell plasmolysis, and to design experiments that distinguish between tolerance of salt and tolerance of water stress.

5,868 citations

"Constitutive Expression of a miR319..." refers background in this paper

  • ...Plant responses to drought and salt stresses have been studied extensively in understanding the physiological and molecular mechanisms underlying plant adaptation to abiotic stress (Munns, 2002; Wang et al., 2003; Chaves et al., 2009)....

    [...]

Journal Article•DOI•
Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance

[...]

Wangxia Wang1, Basia Vinocur1, Arie Altman1•
Hebrew University of Jerusalem1
26 Sep 2003-Planta
TL;DR: The present review summarizes the recent advances in elucidating stress-response mechanisms and their biotechnological applications and examines the following aspects: regulatory controls, metabolite engineering, ion transport, antioxidants and detoxification, late embryogenesis abundant (LEA) and heat-shock proteins.
Abstract: Abiotic stresses, such as drought, salinity, extreme temperatures, chemical toxicity and oxidative stress are serious threats to agriculture and the natural status of the environment. Increased salinization of arable land is expected to have devastating global effects, resulting in 30% land loss within the next 25 years, and up to 50% by the year 2050. Therefore, breeding for drought and salinity stress tolerance in crop plants (for food supply) and in forest trees (a central component of the global ecosystem) should be given high research priority in plant biotechnology programs. Molecular control mechanisms for abiotic stress tolerance are based on the activation and regulation of specific stress-related genes. These genes are involved in the whole sequence of stress responses, such as signaling, transcriptional control, protection of membranes and proteins, and free-radical and toxic-compound scavenging. Recently, research into the molecular mechanisms of stress responses has started to bear fruit and, in parallel, genetic modification of stress tolerance has also shown promising results that may ultimately apply to agriculturally and ecologically important plants. The present review summarizes the recent advances in elucidating stress-response mechanisms and their biotechnological applications. Emphasis is placed on transgenic plants that have been engineered based on different stress-response mechanisms. The review examines the following aspects: regulatory controls, metabolite engineering, ion transport, antioxidants and detoxification, late embryogenesis abundant (LEA) and heat-shock proteins.

3,248 citations

"Constitutive Expression of a miR319..." refers background in this paper

  • ...Plant responses to drought and salt stresses have been studied extensively in understanding the physiological and molecular mechanisms underlying plant adaptation to abiotic stress (Munns, 2002; Wang et al., 2003; Chaves et al., 2009)....

    [...]

Journal Article•DOI•
Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell

[...]

Maria Manuela Chaves1, Jaume Flexas, Carla Pinheiro2•
Instituto Superior de Agronomia1, Universidade Nova de Lisboa2
01 Feb 2009-Annals of Botany
TL;DR: It is becoming apparent that plants perceive and respond to drought and salt stresses by quickly altering gene expression in parallel with physiological and biochemical alterations; this occurs even under mild to moderate stress conditions.

3,080 citations

"Constitutive Expression of a miR319..." refers background in this paper

  • ...Plant responses to drought and salt stresses have been studied extensively in understanding the physiological and molecular mechanisms underlying plant adaptation to abiotic stress (Munns, 2002; Wang et al., 2003; Chaves et al., 2009)....

    [...]

  • ...Photosynthesis is one of the primary processes affected when plants are subjected to environmental stress (Munns et al., 2006; Chaves et al., 2009)....

    [...]

  • ...Plants subjected to drought and salinity experience a physiological water deficit that alters photosynthesis and cell growth and induces osmotic adjustment to maintain current water uptake and cell turgor (Chaves et al., 2009)....

    [...]

Journal Article•DOI•
Na+ Tolerance and Na+ Transport in Higher Plants

[...]

Mark Tester1, Romola Davenport•
University of Cambridge1
01 Apr 2003-Annals of Botany
TL;DR: This work suggests that equally important in a wide range of conditions are processes involving the management of Na(+) movements within the plant, and requires more knowledge of cell-specific transport processes and the consequences of manipulation of transporters and signalling elements in specific cell types.

2,998 citations

"Constitutive Expression of a miR319..." refers background in this paper

  • ...…Hordeum spp., tall wheatgrass, and Triticum tauschii (Yeo and Flowers, 1983; Läuchli, 1984; Tardieu et al., 1992; Bolaños and Edmeades, 1993; Bruce et al., 2002; Munns and James, 2003; Munns et al., 2003; Tester and Davenport, 2003; Campos et al., 2004; Manschadi et al., 2006, 2008; Tardieu, 2012)....

    [...]

Related Papers (5)
Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana.

[...]

01 May 2008-RNA
Han-Hua Liu, Xin Tian, Yan-Jie Li, Changai Wu, Chengchao Zheng 
Novel and Stress-Regulated MicroRNAs and Other Small RNAs from Arabidopsis

[...]

01 Aug 2004-The Plant Cell
Ramanjulu Sunkar, Jian-Kang Zhu
MicroRNAs: Genomics, Biogenesis, Mechanism, and Function

[...]

23 Jan 2004-Cell
David P. Bartel
Control of leaf morphogenesis by microRNAs

[...]

18 Sep 2003-Nature
Javier F. Palatnik, Javier F. Palatnik, Edwards Allen, Xuelin Wu, Carla Schommer, Rebecca Schwab, James C. Carrington, Detlef Weigel, Detlef Weigel 
Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants

[...]

01 Feb 2012-Biochimica et Biophysica Acta
Basel Khraiwesh, Jian-Kang Zhu, Jian-Kang Zhu, Jianhua Zhu