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Special Issue "Mapping Abiotic Stress-Tolerance Genes in Plants"

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (30 September 2019).

Special Issue Editor

Dr. Richard R.-C. Wang
Website
Guest Editor
Forage and Range Research Lab, Utah State University, Logan, UT 84322-6300, USA
Interests: molecular markers; salinity tolerance; disease resistance; DNA sequencing; genome; chromosome; evolution; genetics
Special Issues and Collections in MDPI journals

Special Issue Information

Dear Colleagues,

Tolerance to abiotic stresses caused by environmental conditions can prevent yield loss in crops for sustaining agricultural productivity. For each crop or plant species, there are many abiotic threats such as changes in temperature, soil salinity, water shortage, and soil contaminants. Plants need to posses genes conferring tolerance to these abiotic stresses to adapt to the changing environment in which they are being grown. Foreseeing climate changes, plant breeders are undertaking efforts to identify and transfer genes for tolerance to high/low temperature, soil salinity/alkalinity, drought, or heavy metals, into new cultivars. Plant molecular geneticists have identified many physiological pathways and mechanisms involved in tolerance to various abiotic stresses in some plant species. Many metabolites, enzymes, and transcription factors associated with tolerance to these abiotic stresses have been identified. With the advent of whole-genome sequencing in many important crops, it is time to map the detailed chromosomal locations of known genes that are involved in conferring  tolerance to various abiotic stresses in each crop.

Dr. Richard R.-C. Wang
Guest Editor

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Keywords

  • Tolerance
  • Heat
  • Cold
  • Drought
  • Salinity
  • Whole-genome sequencing
  • Linkage map

Published Papers (22 papers)

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Editorial

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Open AccessEditorial
Chromosomal Distribution of Genes Conferring Tolerance to Abiotic Stresses Versus That of Genes Controlling Resistance to Biotic Stresses in Plants
Int. J. Mol. Sci. 2020, 21(5), 1820; https://doi.org/10.3390/ijms21051820 - 06 Mar 2020
Abstract
Tolerance to abiotic stresses caused by environmental conditions can prevent yield loss in crops for sustaining agricultural productivity [...] Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)

Research

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Open AccessArticle
Bioinformatics Analysis of the Lipoxygenase Gene Family in Radish (Raphanus sativus) and Functional Characterization in Response to Abiotic and Biotic Stresses
Int. J. Mol. Sci. 2019, 20(23), 6095; https://doi.org/10.3390/ijms20236095 - 03 Dec 2019
Cited by 5
Abstract
Lipoxygenases (LOXs) are non-heme iron-containing dioxygenases involved in many developmental and stress-responsive processes in plants. However, little is known about the radish LOX gene family members and their functions in response to biotic and abiotic stresses. In this study, we completed a genome-wide [...] Read more.
Lipoxygenases (LOXs) are non-heme iron-containing dioxygenases involved in many developmental and stress-responsive processes in plants. However, little is known about the radish LOX gene family members and their functions in response to biotic and abiotic stresses. In this study, we completed a genome-wide analysis and expression profiling of RsLOX genes under abiotic and biotic stress conditions. We identified 11 RsLOX genes, which encoded conserved domains, and classified them in 9-LOX and 13-LOX categories according to their phylogenetic relationships. The characteristic structural features of 9-LOX and 13-LOX genes and the encoded protein domains as well as their evolution are presented herein. A qRT-PCR analysis of RsLOX expression levels in the roots under simulated drought, salinity, heat, and cold stresses, as well as in response to a Plasmodiophora brassicae infection, revealed three tandem-clustered RsLOX genes that are involved in responses to various environmental stresses via the jasmonic acid pathway. Our findings provide insights into the evolution and potential biological roles of RsLOXs related to the adaptation of radish to stress conditions. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Functional Analysis of the Soybean GmCDPK3 Gene Responding to Drought and Salt Stresses
Int. J. Mol. Sci. 2019, 20(23), 5909; https://doi.org/10.3390/ijms20235909 - 25 Nov 2019
Cited by 3
Abstract
Plants have a series of response mechanisms to adapt when they are subjected to external stress. Calcium-dependent protein kinases (CDPKs) in plants function against a variety of abiotic stresses. We screened 17 CDPKs from drought- and salt-induced soybean transcriptome sequences. The phylogenetic tree [...] Read more.
Plants have a series of response mechanisms to adapt when they are subjected to external stress. Calcium-dependent protein kinases (CDPKs) in plants function against a variety of abiotic stresses. We screened 17 CDPKs from drought- and salt-induced soybean transcriptome sequences. The phylogenetic tree divided CDPKs of rice, Arabidopsis and soybean into five groups (I–V). Cis-acting element analysis showed that the 17 CDPKs contained some elements associated with drought and salt stresses. Quantitative real-time PCR (qRT-PCR) analysis indicated that the 17 CDPKs were responsive after different degrees of induction under drought and salt stresses. GmCDPK3 was selected as a further research target due to its high relative expression. The subcellular localization experiment showed that GmCDPK3 was located on the membrane of Arabidopsis mesophyll protoplasts. Overexpression of GmCDPK3 improved drought and salt resistance in Arabidopsis. In the soybean hairy roots experiment, the leaves of GmCDPK3 hairy roots with RNA interference (GmCDPK3-RNAi) soybean lines were more wilted than those of GmCDPK3 overexpression (GmCDPK3-OE) soybean lines after drought and salt stresses. The trypan blue staining experiment further confirmed that cell membrane damage of GmCDPK3-RNAi soybean leaves was more severe than in GmCDPK3-OE soybean lines. In addition, proline (Pro) and chlorophyll contents were increased and malondialdehyde (MDA) content was decreased in GmCDPK3-OE soybean lines. On the contrary, GmCDPK3-RNAi soybean lines had decreased Pro and chlorophyll content and increased MDA. The results indicate that GmCDPK3 is essential in resisting drought and salt stresses. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Genome-Wide Identification and Characterization of FBA Gene Family in Polyploid Crop Brassica napus
Int. J. Mol. Sci. 2019, 20(22), 5749; https://doi.org/10.3390/ijms20225749 - 15 Nov 2019
Cited by 3
Abstract
Fructose-1,6-bisphosphate aldolase (FBA) is a versatile metabolic enzyme involved in multiple important processes of glycolysis, gluconeogenesis, and Calvin cycle. Despite its significance in plant biology, the identity of this gene family in oil crops is lacking. Here, we performed genome-wide identification and characterization [...] Read more.
Fructose-1,6-bisphosphate aldolase (FBA) is a versatile metabolic enzyme involved in multiple important processes of glycolysis, gluconeogenesis, and Calvin cycle. Despite its significance in plant biology, the identity of this gene family in oil crops is lacking. Here, we performed genome-wide identification and characterization of FBAs in an allotetraploid species, oilseed rape Brassica napus. Twenty-two BnaFBA genes were identified and divided into two groups based on integrative analyses of functional domains, phylogenetic relationships, and gene structures. Twelve and ten B. napus FBAs (BnaFBAs) were predicted to be localized in the chloroplast and cytoplasm, respectively. Notably, synteny analysis revealed that Brassica-specific triplication contributed to the expansion of the BnaFBA gene family during the evolution of B. napus. Various cis-acting regulatory elements pertinent to abiotic and biotic stresses, as well as phytohormone responses, were detected. Intriguingly, each of the BnaFBA genes exhibited distinct sequence polymorphisms. Among them, six contained signatures of selection, likely having experienced breeding selection during adaptation and domestication. Importantly, BnaFBAs showed diverse expression patterns at different developmental stages and were preferentially highly expressed in photosynthetic tissues. Our data thus provided the foundation for further elucidating the functional roles of individual BnaFBA and also potential targets for engineering to improve photosynthetic productivity in B. napus. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Characterizing the Role of TaWRKY13 in Salt Tolerance
Int. J. Mol. Sci. 2019, 20(22), 5712; https://doi.org/10.3390/ijms20225712 - 14 Nov 2019
Cited by 5
Abstract
The WRKY transcription factor superfamily is known to participate in plant growth and stress response. However, the role of this family in wheat (Triticum aestivum L.) is largely unknown. Here, a salt-induced gene TaWRKY13 was identified in an RNA-Seq data set from [...] Read more.
The WRKY transcription factor superfamily is known to participate in plant growth and stress response. However, the role of this family in wheat (Triticum aestivum L.) is largely unknown. Here, a salt-induced gene TaWRKY13 was identified in an RNA-Seq data set from salt-treated wheat. The results of RT-qPCR analysis showed that TaWRKY13 was significantly induced in NaCl-treated wheat and reached an expression level of about 22-fold of the untreated wheat. Then, a further functional identification was performed in both Arabidopsis thaliana and Oryza sativa L. Subcellular localization analysis indicated that TaWRKY13 is a nuclear-localized protein. Moreover, various stress-related regulatory elements were predicted in the promoter. Expression pattern analysis revealed that TaWRKY13 can also be induced by polyethylene glycol (PEG), exogenous abscisic acid (ABA), and cold stress. After NaCl treatment, overexpressed Arabidopsis lines of TaWRKY13 have a longer root and a larger root surface area than the control (Columbia-0). Furthermore, TaWRKY13 overexpression rice lines exhibited salt tolerance compared with the control, as evidenced by increased proline (Pro) and decreased malondialdehyde (MDA) contents under salt treatment. The roots of overexpression lines were also more developed. These results demonstrate that TaWRKY13 plays a positive role in salt stress. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Genome-Wide Analysis of the DYW Subgroup PPR Gene Family and Identification of GmPPR4 Responses to Drought Stress
Int. J. Mol. Sci. 2019, 20(22), 5667; https://doi.org/10.3390/ijms20225667 - 12 Nov 2019
Cited by 4
Abstract
Pentatricopeptide-repeat (PPR) proteins were identified as a type of nucleus coding protein that is composed of multiple tandem repeats. It has been reported that PPR genes play an important role in RNA editing, plant growth and development, and abiotic stresses in plants. However, [...] Read more.
Pentatricopeptide-repeat (PPR) proteins were identified as a type of nucleus coding protein that is composed of multiple tandem repeats. It has been reported that PPR genes play an important role in RNA editing, plant growth and development, and abiotic stresses in plants. However, the functions of PPR proteins remain largely unknown in soybean. In this study, 179 DYW subgroup PPR genes were identified in soybean genome (Glycine max Wm82.a2.v1). Chromosomal location analysis indicated that DYW subgroup PPR genes were mapped to all 20 chromosomes. Phylogenetic relationship analysis revealed that DYW subgroup PPR genes were categorized into three distinct Clusters (I to III). Gene structure analysis showed that most PPR genes were featured by a lack of intron. Gene duplication analysis demonstrated 30 PPR genes (15 pairs; ~35.7%) were segmentally duplicated among Cluster I PPR genes. Furthermore, we validated the mRNA expression of three genes that were highly up-regulated in soybean drought- and salt-induced transcriptome database and found that the expression levels of GmPPR4 were induced under salt and drought stresses. Under drought stress condition, GmPPR4-overexpressing (GmPPR4-OE) plants showed delayed leaf rolling; higher content of proline (Pro); and lower contents of H2O2, O2 and malondialdehyde (MDA) compared with the empty vector (EV)-control plants. GmPPR4-OE plants exhibited increased transcripts of several drought-inducible genes compared with EV-control plants. Our results provided a comprehensive analysis of the DYW subgroup PPR genes and an insight for improving the drought tolerance in soybean. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Cloning and Expression Analysis of the BocMBF1c Gene Involved in Heat Tolerance in Chinese Kale
Int. J. Mol. Sci. 2019, 20(22), 5637; https://doi.org/10.3390/ijms20225637 - 11 Nov 2019
Cited by 1
Abstract
Chinese kale (Brassica oleracea var. chinensis Lei) is an important vegetable crop in South China, valued for its nutritional content and taste. Nonetheless, the thermal tolerance of Chinese kale still needs improvement. Molecular characterization of Chinese kale’s heat stress response could [...] Read more.
Chinese kale (Brassica oleracea var. chinensis Lei) is an important vegetable crop in South China, valued for its nutritional content and taste. Nonetheless, the thermal tolerance of Chinese kale still needs improvement. Molecular characterization of Chinese kale’s heat stress response could provide a timely solution for developing a thermally tolerant Chinese kale variety. Here, we report the cloning of multi-protein bridging factor (MBF) 1c from Chinese kale (BocMBF1c), an ortholog to the key heat stress responsive gene MBF1c. Phylogenetic analysis showed that BocMBF1c is highly similar to the stress-response transcriptional coactivator MBF1c from Arabidopsis thaliana (AtMBF1c), and the BocMBF1c coding region conserves MBF1 and helix-turn-helix (HTH) domains. Moreover, the promoter region of BocMBF1c contains three heat shock elements (HSEs) and, thus, is highly responsive to heat treatment. This was verified in Nicotiana benthamiana leaf tissue using a green fluorescent protein (GFP) reporter. In addition, the expression of BocMBF1c can be induced by various abiotic stresses in Chinese kale which indicates the involvement of stress responses. The BocMBF1c-eGFP (enhanced green fluorescent protein) chimeric protein quickly translocated into the nucleus under high temperature treatment in Nicotiana benthamiana leaf tissue. Overexpression of BocMBF1c in Arabidopsis thaliana results in a larger size and enhanced thermal tolerance compared with the wild type. Our results provide valuable insight for the role of BocMBF1c during heat stress in Chinese kale. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Comparative Genome-wide Analysis and Expression Profiling of Histone Acetyltransferase (HAT) Gene Family in Response to Hormonal Applications, Metal and Abiotic Stresses in Cotton
Int. J. Mol. Sci. 2019, 20(21), 5311; https://doi.org/10.3390/ijms20215311 - 25 Oct 2019
Cited by 4
Abstract
Post-translational modifications are involved in regulating diverse developmental processes. Histone acetyltransferases (HATs) play vital roles in the regulation of chromation structure and activate the gene transcription implicated in various cellular processes. However, HATs in cotton, as well as their regulation in response to [...] Read more.
Post-translational modifications are involved in regulating diverse developmental processes. Histone acetyltransferases (HATs) play vital roles in the regulation of chromation structure and activate the gene transcription implicated in various cellular processes. However, HATs in cotton, as well as their regulation in response to developmental and environmental cues, remain unidentified. In this study, 9 HATs were identified from Gossypium raimondi and Gossypium arboretum, while 18 HATs were identified from Gossypium hirsutum. Based on their amino acid sequences, Gossypium HATs were divided into three groups: CPB, GNAT, and TAFII250. Almost all the HATs within each subgroup share similar gene structure and conserved motifs. Gossypium HATs are unevenly distributed on the chromosomes, and duplication analysis suggests that Gossypium HATs are under strong purifying selection. Gene expression analysis showed that Gossypium HATs were differentially expressed in various vegetative tissues and at different stages of fiber development. Furthermore, all the HATs were differentially regulated in response to various stresses (salt, drought, cold, heavy metal and DNA damage) and hormones (abscisic acid (ABA) and auxin (NAA)). Finally, co-localization of HAT genes with reported quantitative trait loci (QTL) of fiber development were reported. Altogether, these results highlight the functional diversification of HATs in cotton growth and fiber development, as well as in response to different environmental cues. This study enhances our understanding of function of histone acetylation in cotton growth, fiber development, and stress adaptation, which will eventually lead to the long-term improvement of stress tolerance and fiber quality in cotton. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Genome-Wide Identification, Classification, and Expression Analysis of the Hsf Gene Family in Carnation (Dianthus caryophyllus)
Int. J. Mol. Sci. 2019, 20(20), 5233; https://doi.org/10.3390/ijms20205233 - 22 Oct 2019
Cited by 4
Abstract
Heat shock transcription factors (Hsfs) are a class of important transcription factors (TFs) which play crucial roles in the protection of plants from damages caused by various abiotic stresses. The present study aimed to characterize the Hsf genes in carnation (Dianthus caryophyllus [...] Read more.
Heat shock transcription factors (Hsfs) are a class of important transcription factors (TFs) which play crucial roles in the protection of plants from damages caused by various abiotic stresses. The present study aimed to characterize the Hsf genes in carnation (Dianthus caryophyllus), which is one of the four largest cut flowers worldwide. In this study, a total of 17 non-redundant Hsf genes were identified from the D. caryophyllus genome. Specifically, the gene structure and motifs of each DcaHsf were comprehensively analyzed. Phylogenetic analysis of the DcaHsf family distinctly separated nine class A, seven class B, and one class C Hsf genes. Additionally, promoter analysis indicated that the DcaHsf promoters included various cis-acting elements that were related to stress, hormones, as well as development processes. In addition, cis-elements, such as STRE, MYB, and ABRE binding sites, were identified in the promoters of most DcaHsf genes. According to qRT-PCR data, the expression of DcaHsfs varied in eight tissues and six flowering stages and among different DcaHsfs, even in the same class. Moreover, DcaHsf-A1, A2a, A9a, B2a, B3a revealed their putative involvement in the early flowering stages. The time-course expression profile of DcaHsf during stress responses illustrated that all the DcaHsfs were heat- and drought-responsive, and almost all DcaHsfs were down-regulated by cold, salt, and abscisic acid (ABA) stress. Meanwhile, DcaHsf-A3, A7, A9a, A9b, B3a were primarily up-regulated at an early stage in response to salicylic acid (SA). This study provides an overview of the Hsf gene family in D. caryophyllus and a basis for the breeding of stress-resistant carnation. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Genome-Wide Identification and Characterization of Cucumber BPC Transcription Factors and Their Responses to Abiotic Stresses and Exogenous Phytohormones
Int. J. Mol. Sci. 2019, 20(20), 5048; https://doi.org/10.3390/ijms20205048 - 11 Oct 2019
Cited by 1
Abstract
BASIC PENTACYSTEINE (BPC) is a small transcription factor family that functions in diverse growth and development processes in plants. However, the roles of BPCs in plants, especially cucumber (Cucumis sativus L.), in response to abiotic stress and exogenous phytohormones are still unclear. [...] Read more.
BASIC PENTACYSTEINE (BPC) is a small transcription factor family that functions in diverse growth and development processes in plants. However, the roles of BPCs in plants, especially cucumber (Cucumis sativus L.), in response to abiotic stress and exogenous phytohormones are still unclear. Here, we identified four BPC genes in the cucumber genome, and classified them into two groups according to phylogenetic analysis. We also investigated the gene structures and detected five conserved motifs in these CsBPCs. Tissue expression pattern analysis revealed that the four CsBPCs were expressed ubiquitously in both vegetative and reproductive organs. Additionally, the transcriptional levels of the four CsBPCs were induced by various abiotic stress and hormone treatments. Overexpression of CsBPC2 in tobacco (Nicotiana tabacum) inhibited seed germination under saline, polyethylene glycol, and abscisic acid (ABA) conditions. The results suggest that the CsBPC genes may play crucial roles in cucumber growth and development, as well as responses to abiotic stresses and plant hormones. CsBPC2 overexpression in tobacco negatively affected seed germination under hyperosmotic conditions. Additionally, CsBPC2 functioned in ABA-inhibited seed germination and hypersensitivity to ABA-mediated responses. Our results provide fundamental information for further research on the biological functions of BPCs in development and abiotic stress responses in cucumber and other plant species. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Map-Based Functional Analysis of the GhNLP Genes Reveals Their Roles in Enhancing Tolerance to N-Deficiency in Cotton
Int. J. Mol. Sci. 2019, 20(19), 4953; https://doi.org/10.3390/ijms20194953 - 08 Oct 2019
Cited by 2
Abstract
Nitrogen is a key macronutrient needed by plants to boost their production, but the development of cotton genotypes through conventional approaches has hit a bottleneck due to the narrow genetic base of the elite cotton cultivars, due to intensive selection and inbreeding. Based [...] Read more.
Nitrogen is a key macronutrient needed by plants to boost their production, but the development of cotton genotypes through conventional approaches has hit a bottleneck due to the narrow genetic base of the elite cotton cultivars, due to intensive selection and inbreeding. Based on our previous research, in which the BC2F2 generations developed from two upland cotton genotypes, an abiotic stress-tolerant genotype, G. tomentosum (donor parent) and a highly-susceptible, and a highly-susceptible, but very productive, G. hirsutum (recurrent parent), were profiled under drought stress conditions. The phenotypic and the genotypic data generated through genotyping by sequencing (GBS) were integrated to map drought-tolerant quantitative trait loci (QTLs). Within the stable QTLs region for the various drought tolerance traits, a nodule-inception-like protein (NLP) gene was identified. We performed a phylogenetic analysis of the NLP proteins, mapped their chromosomal positions, intron-exon structures and conducted ds/dn analysis, which showed that most NLP genes underwent negative or purifying selection. Moreover, the functions of one of the highly upregulated genes, Gh_A05G3286 (Gh NLP5), were evaluated using the virus gene silencing (VIGS) mechanism. A total of 226 proteins encoded by the NLP genes were identified, with 105, 61, and 60 in Gossypium hirsutum, G. raimondii, and G. arboreum, respectively. Comprehensive Insilico analysis revealed that the proteins encoded by the NLP genes had varying molecular weights, protein lengths, isoelectric points (pI), and grand hydropathy values (GRAVY). The GRAVY values ranged from a negative one to zero, showing that proteins were hydrophilic. Moreover, various cis-regulatory elements that are the binding sites for stress-associated transcription factors were found in the promoters of various NLP genes. In addition, many miRNAs were predicted to target NLP genes, notably miR167a, miR167b, miR160, and miR167 that were previously shown to target five NAC genes, including NAC1 and CUC1, under N-limited conditions. The real-time quantitative polymerase chain reaction (RT-qPCR) analysis, revealed that five genes, Gh_D02G2018, Gh_A12G0439, Gh_A03G0493, Gh_A03G1178, and Gh_A05G3286 were significantly upregulated and perhaps could be the key NLP genes regulating plant response under N-limited conditions. Furthermore, the knockdown of the Gh_A05G3286 (GhNLP5) gene by virus-induced silencing (VIGS) significantly reduced the ability of these plants to the knockdown of the Gh_A05G3286 (GhNLP5) gene by virus-induced gene silencing (VIGS) significantly reduced the ability of the VIGS-plants to tolerate N-limited conditions compared to the wild types (WT). The VIGS-plants registered lower chlorophyll content, fresh shoot biomass, and fresh root biomass, addition to higher levels of malondialdehyde (MDA) and significantly reduced levels of proline, and superoxide dismutase (SOD) compared to the WT under N-limited conditions. Subsequently, the expression levels of the Nitrogen-stress responsive genes, GhTap46, GhRPL18A, and GhKLU were shown to be significantly downregulated in VIGS-plants compared to their WT under N-limited conditions. The downregulation of the nitrogen-stress responsive genes provided evidence that the silenced gene had an integral role in enhancing cotton plant tolerance to N-limited conditions. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Overexpression of GmCAMTA12 Enhanced Drought Tolerance in Arabidopsis and Soybean
Int. J. Mol. Sci. 2019, 20(19), 4849; https://doi.org/10.3390/ijms20194849 - 29 Sep 2019
Cited by 9
Abstract
Fifteen transcription factors in the CAMTA (calmodulin binding transcription activator) family of soybean were reported to differentially regulate in multiple stresses; however, their functional analyses had not yet been attempted. To characterize their role in stresses, we first comprehensively analyzed the GmCAMTA family [...] Read more.
Fifteen transcription factors in the CAMTA (calmodulin binding transcription activator) family of soybean were reported to differentially regulate in multiple stresses; however, their functional analyses had not yet been attempted. To characterize their role in stresses, we first comprehensively analyzed the GmCAMTA family in silico and thereafter determined their expression pattern under drought. The bioinformatics analysis revealed multiple stress-related cis-regulatory elements including ABRE, SARE, G-box and W-box, 10 unique miRNA (microRNA) targets in GmCAMTA transcripts and 48 proteins in GmCAMTAs’ interaction network. We then cloned the 2769 bp CDS (coding sequence) of GmCAMTA12 in an expression vector and overexpressed in soybean and Arabidopsis through Agrobacterium-mediated transformation. The T3 (Transgenic generation 3) stably transformed homozygous lines of Arabidopsis exhibited enhanced tolerance to drought in soil as well as on MS (Murashige and Skoog) media containing mannitol. In their drought assay, the average survival rate of transgenic Arabidopsis lines OE5 and OE12 (Overexpression Line 5 and Line 12) was 83.66% and 87.87%, respectively, which was ~30% higher than that of wild type. In addition, the germination and root length assays as well as physiological indexes such as proline and malondialdehyde contents, catalase activity and leakage of electrolytes affirmed the better performance of OE lines. Similarly, GmCAMTA12 overexpression in soybean promoted drought-efficient hairy roots in OE chimeric plants as compare to that of VC (Vector control). In parallel, the improved growth performance of OE in Hoagland-PEG (polyethylene glycol) and on MS-mannitol was revealed by their phenotypic, physiological and molecular measures. Furthermore, with the overexpression of GmCAMTA12, the downstream genes including AtAnnexin5, AtCaMHSP, At2G433110 and AtWRKY14 were upregulated in Arabidopsis. Likewise, in soybean hairy roots, GmELO, GmNAB and GmPLA1-IId were significantly upregulated as a result of GmCAMTA12 overexpression and majority of these upregulated genes in both plants possess CAMTA binding CGCG/CGTG motif in their promoters. Taken together, we report that GmCAMTA12 plays substantial role in tolerance of soybean against drought stress and could prove to be a novel candidate for engineering soybean and other plants against drought stress. Some research gaps were also identified for future studies to extend our comprehension of Ca-CaM-CAMTA-mediated stress regulatory mechanisms. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Arabidopsis NDL-AGB1 modules Play Role in Abiotic Stress and Hormonal Responses Along with Their Specific Functions
Int. J. Mol. Sci. 2019, 20(19), 4736; https://doi.org/10.3390/ijms20194736 - 24 Sep 2019
Cited by 1
Abstract
Arabidopsis N-MYC Downregulated Like Proteins (NDLs) are interacting partners of G-Protein core components. Animal homologs of the gene family N-myc downstream regulated gene (NDRG) has been found to be induced during hypoxia, DNA damage, in presence of reducing agent, increased intracellular calcium level [...] Read more.
Arabidopsis N-MYC Downregulated Like Proteins (NDLs) are interacting partners of G-Protein core components. Animal homologs of the gene family N-myc downstream regulated gene (NDRG) has been found to be induced during hypoxia, DNA damage, in presence of reducing agent, increased intracellular calcium level and in response to metal ions like nickel and cobalt, which indicates the involvement of the gene family during stress responses. Arabidopsis NDL gene family contains three homologs NDL1, NDL2 and NDL3 which share up to 75% identity at protein level. Previous studies on NDL proteins involved detailed characterization of the role of NDL1; roles of other two members were also established in root and shoot development using miRNA knockdown approach. Role of entire family in development has been established but specific functions of NDL2 and NDL3 if any are still unknown. Our in-silico analysis of NDLs promoters reveled that all three members share some common and some specific transcription factors (TFs) binding sites, hinting towards their common as well as specific functions. Based on promoter elements characteristics, present study was designed to carry out comparative analysis of the Arabidopsis NDL family during different stages of plant development, under various abiotic stresses and plant hormonal responses, in order to find out their specific and combined roles in plant growth and development. Developmental analysis using GUS fusion revealed specific localization/expression during different stages of development for all three family members. Stress analysis after treatment with various hormonal and abiotic stresses showed stress and tissue-specific differential expression patterns for all three NDL members. All three NDL members were collectively showed role in dehydration stress along with specific responses to various treatments. Their specific expression patterns were affected by presence of interacting partner the Arabidopsis heterotrimeric G-protein β subunit 1 (AGB1). The present study will improve our understanding of the possible molecular mechanisms of action of the independent NDLAGB1 modules during stress and hormonal responses. These findings also suggest potential use of this knowledge for crop improvement. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Identification and Expression Analysis of GRAS Transcription Factors to Elucidate Candidate Genes Related to Stolons, Fruit Ripening and Abiotic Stresses in Woodland Strawberry (Fragaria vesca)
Int. J. Mol. Sci. 2019, 20(18), 4593; https://doi.org/10.3390/ijms20184593 - 17 Sep 2019
Cited by 4
Abstract
The cultivated strawberry (Fragaria × ananassa), an allo-octoploid with non-climacteric fleshy fruits, is a popular Rosaceae horticultural crop worldwide that is mainly propagated via stolons during cultivation. Woodland strawberry (Fragaria vesca), one of the four diploid progenitor species of [...] Read more.
The cultivated strawberry (Fragaria × ananassa), an allo-octoploid with non-climacteric fleshy fruits, is a popular Rosaceae horticultural crop worldwide that is mainly propagated via stolons during cultivation. Woodland strawberry (Fragaria vesca), one of the four diploid progenitor species of cultivated strawberry, is widely used as a model plant in the study of Rosaceae fruit trees, non-climacteric fruits and stolons. One GRAS transcription factor has been shown to regulate stolon formation; the other GRAS proteins in woodland strawberry remain unknown. In this study, we identified 54 FveGRAS proteins in woodland strawberry, and divided them into 14 subfamilies. Conserved motif analysis revealed that the motif composition of FveGRAS proteins was conserved within each subfamily, but diverged widely among subfamilies. We found 56 orthologous pairs of GRAS proteins between woodland strawberry and Arabidopsis thaliana, 47 orthologous pairs between woodland strawberry and rice and 92 paralogous pairs within woodland strawberry. The expression patterns of FveGRAS genes in various organs and tissues, and changes therein under cold, heat and GA3 treatments, were characterized using transcriptomic analysis. The results showed that 34 FveGRAS genes were expressed with different degrees in at least four organs, including stolons; only a few genes displayed organ-specific expression. The expression levels of 16 genes decreased, while that of four genes increased during fruit ripening; FveGRAS54 showed the largest increase in expression. Under cold, heat and GA3 treatments, around half of the FveGRAS genes displayed increased or decreased expression to some extent, suggesting differing functions of these FveGRAS genes in the responses to cold, heat and GAs. This study provides insight into the potential functions of FveGRAS genes in woodland strawberry. A few FveGRAS genes were identified as candidate genes for further study, in terms of their functions in stolon formation, fruit ripening and abiotic stresses. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
QTL Analysis of Resistance to High-Intensity UV-B Irradiation in Soybean (Glycine max [L.] Merr.)
Int. J. Mol. Sci. 2019, 20(13), 3287; https://doi.org/10.3390/ijms20133287 - 04 Jul 2019
Cited by 1
Abstract
High-intensity ultraviolet-B (UV-B) irradiation is a complex abiotic stressor resulting in excessive light exposure, heat, and dehydration, thereby affecting crop yields. In the present study, we identified quantitative trait loci (QTLs) for resistance to high-intensity UV-B irradiation in soybean (Glycine max [L.]). [...] Read more.
High-intensity ultraviolet-B (UV-B) irradiation is a complex abiotic stressor resulting in excessive light exposure, heat, and dehydration, thereby affecting crop yields. In the present study, we identified quantitative trait loci (QTLs) for resistance to high-intensity UV-B irradiation in soybean (Glycine max [L.]). We used a genotyping-by-sequencing approach using an F6 recombinant inbred line (RIL) population derived from a cross between Cheongja 3 (UV-B sensitive) and Buseok (UV-B resistant). We evaluated the degree of leaf damage by high-intensity UV-B radiation in the RIL population and identified four QTLs, UVBR12-1, 6-1, 10-1, and 14-1, for UV-B stress resistance, together explaining 20% of the observed phenotypic variation. The genomic regions containing UVBR12-1 and UVBR6-1 and their syntenic blocks included other known biotic and abiotic stress-related QTLs. The QTL with the highest logarithm of odds (LOD) score of 3.76 was UVBR12-1 on Chromosome 12, containing two genes encoding spectrin beta chain, brain (SPTBN, Glyma.12g088600) and bZIP transcription factor21/TGACG motif-binding 9 (bZIP TF21/TGA9, Glyma.12g088700). Their amino acid sequences did not differ between the mapping parents, but both genes were significantly upregulated by UV-B stress in Buseok but not in Cheongja 3. Among five genes in UVBR6-1 on Chromosome 6, Glyma.06g319700 (encoding a leucine-rich repeat family protein) had two nonsynonymous single nucleotide polymorphisms differentiating the parental lines. Our findings offer powerful genetic resources for efficient and precise breeding programs aimed at developing resistant soybean cultivars to multiple stresses. Furthermore, functional validation of the candidate genes will improve our understanding of UV-B stress defense mechanisms. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
A Stress-Responsive NAC Transcription Factor from Tiger Lily (LlNAC2) Interacts with LlDREB1 and LlZHFD4 and Enhances Various Abiotic Stress Tolerance in Arabidopsis
Int. J. Mol. Sci. 2019, 20(13), 3225; https://doi.org/10.3390/ijms20133225 - 30 Jun 2019
Cited by 7
Abstract
Our previous studies have indicated that a partial NAC domain protein gene is strongly up-regulated by cold stress (4 °C) in tiger lily (Lilium lancifolium). In this study, we cloned the full-length of this NAC gene, LlNAC2, to further investigate [...] Read more.
Our previous studies have indicated that a partial NAC domain protein gene is strongly up-regulated by cold stress (4 °C) in tiger lily (Lilium lancifolium). In this study, we cloned the full-length of this NAC gene, LlNAC2, to further investigate the function of LlNAC2 in response to various abiotic stresses and the possible involvement in stress tolerance of the tiger lily plant. LlNAC2 was noticeably induced by cold, drought, salt stresses, and abscisic acid (ABA) treatment. Promoter analysis showed that various stress-related cis-acting regulatory elements were located in the promoter of LlNAC2; and the promoter was sufficient to enhance activity of GUS protein under cold, salt stresses and ABA treatment. DREB1 (dehydration-responsive binding protein1) from tiger lily (LlDREB1) was proved to be able to bind to the promoter of LlNAC2 by yeast one-hybrid (Y1H) assay. LlNAC2 was shown to physically interact with LlDREB1 and zinc finger-homeodomain ZFHD4 from the tiger lily (LlZFHD4) by bimolecular fluorescence complementation (BiFC) assay. Overexpressing LlNAC2 in Arabidopsis thaliana showed ABA hypersensitivity and enhanced tolerance to cold, drought, and salt stresses. These findings indicated LlNAC2 is involved in both DREB/CBF-COR and ABA signaling pathways to regulate stress tolerance of the tiger lily. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
A MYB-Related Transcription Factor from Lilium lancifolium L. (LlMYB3) Is Involved in Anthocyanin Biosynthesis Pathway and Enhances Multiple Abiotic Stress Tolerance in Arabidopsis thaliana
Int. J. Mol. Sci. 2019, 20(13), 3195; https://doi.org/10.3390/ijms20133195 - 29 Jun 2019
Cited by 3
Abstract
Most commercial cultivars of lily are sensitive to abiotic stresses. However, tiger lily (Lilium lancifolium L.), one of the most widely distributed wild lilies in Asia, has strong abiotic stresses resistance. Thus, it is indispensable to identify stress-responsive candidate genes in tiger [...] Read more.
Most commercial cultivars of lily are sensitive to abiotic stresses. However, tiger lily (Lilium lancifolium L.), one of the most widely distributed wild lilies in Asia, has strong abiotic stresses resistance. Thus, it is indispensable to identify stress-responsive candidate genes in tiger lily for the stress resistance improvement of plants. In this study, a MYB related homolog (LlMYB3) from tiger lily was functionally characterized as a positive regulator in plant stress tolerance. LlMYB3 is a nuclear protein with transcriptional activation activity at C-terminus. The expression of LlMYB3 gene was induced by multiple stress treatments. Several stress-related cis-acting regulatory elements (MYBRS, MYCRS, LTRE and DRE/CRT) were located within the promoter of LlMYB3; however, the promoter activity was not induced sufficiently by various stresses treatments. Overexpressing LlMYB3 in Arabidopsis thaliana L. transgenic plants showed ABA hypersensitivity and enhanced tolerance to cold, drought, and salt stresses. Furthermore, we found LlMYB3 highly co-expressed with LlCHS2 gene under cold treatment; yeast one-hybrid (Y1H) assays demonstrated LlMYB3 was able to bind to the promoter of LlCHS2. These findings suggest that the stress-responsive LlMYB3 may be involved in anthocyanin biosynthesis pathway to regulate stress tolerance of tiger lily. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Phylogenetic, Molecular, and Functional Characterization of PpyCBF Proteins in Asian Pears (Pyrus pyrifolia)
Int. J. Mol. Sci. 2019, 20(9), 2074; https://doi.org/10.3390/ijms20092074 - 26 Apr 2019
Cited by 3
Abstract
C-repeat binding factor/dehydration-responsive element (CBF/DRE) transcription factors (TFs) participate in a variety of adaptive mechanisms, and are involved in molecular signaling and abiotic stress tolerance in plants. In pear (Pyrus pyrifolia) and other rosaceous crops, the independent evolution of CBF subfamily [...] Read more.
C-repeat binding factor/dehydration-responsive element (CBF/DRE) transcription factors (TFs) participate in a variety of adaptive mechanisms, and are involved in molecular signaling and abiotic stress tolerance in plants. In pear (Pyrus pyrifolia) and other rosaceous crops, the independent evolution of CBF subfamily members requires investigation to understand the possible divergent functions of these proteins. In this study, phylogenetic analysis divided six PpyCBFs from the Asian pear genome into three clades/subtypes, and collinearity and phylogenetic analyses suggested that PpyCBF3 was the mother CBF. All PpyCBFs were found to be highly expressed in response to low temperature, salt, drought, and abscisic acid (ABA) as well as bud endodormancy, similar to PpyCORs (PpyCOR47, PpyCOR15A, PpyRD29A, and PpyKIN). Transcript levels of clade II PpyCBFs during low temperature and ABA treatments were higher than those of clades I and III. Ectopic expression of PpyCBF2 and PpyCBF3 in Arabidopsis enhanced its tolerance against abiotic stresses, especially to low temperature in the first case and salt and drought stresses in the latter, and resulted in lower reactive oxygen species (ROS) and antioxidant gene activities compared with the wild type. The increased expression of endogenous ABA-dependent and -independent genes during normal conditions in PpyCBF2- and PpyCBF3-overexpressing Arabidopsis lines suggested that PpyCBFs were involved in both ABA-dependent and -independent pathways. All PpyCBFs, especially the mother CBF, had high transactivation activities with 6XCCGAC binding elements. Luciferase and Y1H assays revealed the existence of phylogenetically and promoter-dependent conserved CBF–COR cascades in the pear. The presence of a previously identified CCGA binding site, combined with the results of mutagenesis of the CGACA binding site of the PpyCOR15A promoter, indicated that CGA was a core binding element of PpyCBFs. In conclusion, PpyCBF TFs might operate redundantly via both ABA-dependent and -independent pathways, and are strongly linked to abiotic stress signaling and responses in the Asian pear. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
Deep Transcriptome Analysis Reveals Reactive Oxygen Species (ROS) Network Evolution, Response to Abiotic Stress, and Regulation of Fiber Development in Cotton
Int. J. Mol. Sci. 2019, 20(8), 1863; https://doi.org/10.3390/ijms20081863 - 15 Apr 2019
Cited by 9
Abstract
Reactive oxygen species (ROS) are important molecules in the plant, which are involved in many biological processes, including fiber development and adaptation to abiotic stress in cotton. We carried out transcription analysis to determine the evolution of the ROS genes and analyzed their [...] Read more.
Reactive oxygen species (ROS) are important molecules in the plant, which are involved in many biological processes, including fiber development and adaptation to abiotic stress in cotton. We carried out transcription analysis to determine the evolution of the ROS genes and analyzed their expression levels in various tissues of cotton plant under abiotic stress conditions. There were 515, 260, and 261 genes of ROS network that were identified in Gossypium hirsutum (AD1 genome), G. arboreum (A genome), and G. raimondii (D genome), respectively. The ROS network genes were found to be distributed in all the cotton chromosomes, but with a tendency of aggregating on either the lower or upper arms of the chromosomes. Moreover, all the cotton ROS network genes were grouped into 17 families as per the phylogenetic tress analysis. A total of 243 gene pairs were orthologous in G. arboreum and G. raimondii. There were 240 gene pairs that were orthologous in G. arboreum, G. raimondii, and G. hirsutum. The synonymous substitution value (Ks) peaks of orthologous gene pairs between the At subgenome and the A progenitor genome (G. arboreum), D subgenome and D progenitor genome (G. raimondii) were 0.004 and 0.015, respectively. The Ks peaks of ROS network orthologous gene pairs between the two progenitor genomes (A and D genomes) and two subgenomes (At and Dt subgenome) were 0.045. The majority of Ka/Ks value of orthologous gene pairs between the A, D genomes and two subgenomes of TM-1 were lower than 1.0. RNA seq. analysis and RT-qPCR validation, showed that, CSD1,2,3,5,6; FSD1,2; MSD1,2; APX3,11; FRO5.6; and RBOH6 played a major role in fiber development while CSD1, APX1, APX2, MDAR1, GPX4-6-7, FER2, RBOH6, RBOH11, and FRO5 were integral for enhancing salt stress in cotton. ROS network-mediated signal pathway enhances the mechanism of fiber development and regulation of abiotic stress in Gossypium. This study will enhance the understanding of ROS network and form the basic foundation in exploring the mechanism of ROS network-involving the fiber development and regulation of abiotic stress in cotton. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessArticle
HvPAA1 Encodes a P-Type ATPase, a Novel Gene for Cadmium Accumulation and Tolerance in Barley (Hordeum vulgare L.)
Int. J. Mol. Sci. 2019, 20(7), 1732; https://doi.org/10.3390/ijms20071732 - 08 Apr 2019
Cited by 4
Abstract
The identification of gene(s) that are involved in Cd accumulation/tolerance is vital in developing crop cultivars with low Cd accumulation. We developed a doubled haploid (DH) population that was derived from a cross of Suyinmai 2 (Cd-sensitive) × Weisuobuzhi (Cd-tolerant) to conduct quantitative [...] Read more.
The identification of gene(s) that are involved in Cd accumulation/tolerance is vital in developing crop cultivars with low Cd accumulation. We developed a doubled haploid (DH) population that was derived from a cross of Suyinmai 2 (Cd-sensitive) × Weisuobuzhi (Cd-tolerant) to conduct quantitative trait loci (QTL) mapping studies. We assessed chlorophyll content, traits that are associated with development, metal concentration, and antioxidative enzyme activity in DH population lines and parents under control and Cd stress conditions. A single QTL, designated as qShCd7H, was identified on chromosome 7H that was linked to shoot Cd concentration; qShCd7H explained 17% of the phenotypic variation. Comparative genomics, map-based cloning, and gene silencing were used in isolation, cloning, and functional characterization of the candidate gene. A novel gene HvPAA1, being related to shoot Cd concentration, was identified from qShCd7H. Sequence comparison indicated that HvPAA1 carried seven domains with an N-glycosylation motif. HvPAA1 is predominantly expressed in shoots. Subcellular localization verified that HvPAA1 is located in plasma membrane. The silencing of HvPAA1 resulted in growth inhibition, greater Cd accumulation, and a significant decrease in Cd tolerance. We conclude HvPAA1 is a novel plasma membrane-localized ATPase that contributes to Cd tolerance and accumulation in barley. The results provide us with new insights that may aid in the screening and development of Cd-tolerant and low-Cd-accumulation crops. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Review

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Open AccessReview
Stay-Green Trait: A Prospective Approach for Yield Potential, and Drought and Heat Stress Adaptation in Globally Important Cereals
Int. J. Mol. Sci. 2019, 20(23), 5837; https://doi.org/10.3390/ijms20235837 - 20 Nov 2019
Cited by 14
Abstract
The yield losses in cereal crops because of abiotic stress and the expected huge losses from climate change indicate our urgent need for useful traits to achieve food security. The stay-green (SG) is a secondary trait that enables crop plants to maintain their [...] Read more.
The yield losses in cereal crops because of abiotic stress and the expected huge losses from climate change indicate our urgent need for useful traits to achieve food security. The stay-green (SG) is a secondary trait that enables crop plants to maintain their green leaves and photosynthesis capacity for a longer time after anthesis, especially under drought and heat stress conditions. Thus, SG plants have longer grain-filling period and subsequently higher yield than non-SG. SG trait was recognized as a superior characteristic for commercially bred cereal selection to overcome the current yield stagnation in alliance with yield adaptability and stability. Breeding for functional SG has contributed in improving crop yields, particularly when it is combined with other useful traits. Thus, elucidating the molecular and physiological mechanisms associated with SG trait is maybe the key to defeating the stagnation in productivity associated with adaptation to environmental stress. This review discusses the recent advances in SG as a crucial trait for genetic improvement of the five major cereal crops, sorghum, wheat, rice, maize, and barley with particular emphasis on the physiological consequences of SG trait. Finally, we provided perspectives on future directions for SG research that addresses present and future global challenges. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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Open AccessReview
The Adaptive Mechanism of Plants to Iron Deficiency via Iron Uptake, Transport, and Homeostasis
Int. J. Mol. Sci. 2019, 20(10), 2424; https://doi.org/10.3390/ijms20102424 - 16 May 2019
Cited by 16
Abstract
Iron is an essential element for plant growth and development. While abundant in soil, the available Fe in soil is limited. In this regard, plants have evolved a series of mechanisms for efficient iron uptake, allowing plants to better adapt to iron deficient [...] Read more.
Iron is an essential element for plant growth and development. While abundant in soil, the available Fe in soil is limited. In this regard, plants have evolved a series of mechanisms for efficient iron uptake, allowing plants to better adapt to iron deficient conditions. These mechanisms include iron acquisition from soil, iron transport from roots to shoots, and iron storage in cells. The mobilization of Fe in plants often occurs via chelating with phytosiderophores, citrate, nicotianamine, mugineic acid, or in the form of free iron ions. Recent work further elucidates that these genes’ response to iron deficiency are tightly controlled at transcriptional and posttranscriptional levels to maintain iron homeostasis. Moreover, increasing evidences shed light on certain factors that are identified to be interconnected and integrated to adjust iron deficiency. In this review, we highlight the molecular and physiological bases of iron acquisition from soil to plants and transport mechanisms for tolerating iron deficiency in dicotyledonous plants and rice. Full article
(This article belongs to the Special Issue Mapping Abiotic Stress-Tolerance Genes in Plants)
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