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1.  Identification of transcriptome induced in roots of maize seedlings at the late stage of waterlogging 
BMC Plant Biology  2010;10:189.
Background
Plants respond to low oxygen stress, particularly that caused by waterlogging, by altering transcription and translation. Previous studies have mostly focused on revealing the mechanism of the response at the early stage, and there is limited information about the transcriptional profile of genes in maize roots at the late stage of waterlogging. The genetic basis of waterlogging tolerance is largely unknown. In this study, the transcriptome at the late stage of waterlogging was assayed in root cells of the tolerant inbred line HZ32, using suppression subtractive hybridization (SSH). A forward SSH library using RNA populations from four time points (12 h, 16 h, 20 h and 24 h) after waterlogging treatment was constructed to reveal up-regulated genes, and transcriptional and linkage data was integrated to identify candidate genes for waterlogging tolerance.
Results
Reverse Northern analysis of a set of 768 cDNA clones from the SSH library revealed a large number of genes were up-regulated by waterlogging. A total of 465 ESTs were assembled into 296 unigenes. Bioinformatic analysis revealed that the genes were involved in complex pathways, such as signal transduction, protein degradation, ion transport, carbon and amino acid metabolism, and transcriptional and translational regulation, and might play important roles at the late stage of the response to waterlogging. A significant number of unigenes were of unknown function. Approximately 67% of the unigenes could be aligned on the maize genome and 63 of them were co-located within reported QTLs.
Conclusion
The late response to waterlogging in maize roots involves a broad spectrum of genes, which are mainly associated with two response processes: defense at the early stage and adaption at the late stage. Signal transduction plays a key role in activating genes related to the tolerance mechanism for survival during prolonged waterlogging. The crosstalk between carbon and amino acid metabolism reveals that amino acid metabolism performs two main roles at the late stage: the regulation of cytoplasmic pH and energy supply through breakdown of the carbon skeleton.
doi:10.1186/1471-2229-10-189
PMCID: PMC2956539  PMID: 20738849
2.  Dynamic QTL Analysis and Candidate Gene Mapping for Waterlogging Tolerance at Maize Seedling Stage 
PLoS ONE  2013;8(11):e79305.
Soil waterlogging is one of the major abiotic stresses adversely affecting maize growth and yield. To identify dynamic expression of genes or quantitative trait loci (QTL), QTL associated with plant height, root length, root dry weight, shoot dry weight and total dry weight were identified via conditional analysis in a mixed linear model and inclusive composite interval mapping method at three respective periods under waterlogging and control conditions. A total of 13, 19 and 23 QTL were detected at stages 3D|0D (the period during 0–3 d of waterlogging), 6D|3D and 9D|6D, respectively. The effects of each QTL were moderate and distributed over nine chromosomes, singly explaining 4.14–18.88% of the phenotypic variation. Six QTL (ph6-1, rl1-2, sdw4-1, sdw7-1, tdw4-1 and tdw7-1) were identified at two consistent stages of seedling development, which could reflect a continuous expression of genes; the remaining QTL were detected at only one stage. Thus, expression of most QTL was influenced by the developmental status. In order to provide additional evidence regarding the role of corresponding genes in waterlogging tolerance, mapping of Expressed Sequence Tags markers and microRNAs were conducted. Seven candidate genes were observed to co-localize with the identified QTL on chromosomes 1, 4, 6, 7 and 9, and may be important candidate genes for waterlogging tolerance. These results are a good starting point for understanding the genetic basis for selectively expressing of QTL in different stress periods and the common genetic control mechanism of the co-localized traits.
doi:10.1371/journal.pone.0079305
PMCID: PMC3828346  PMID: 24244474
3.  Mapping of QTL Associated with Waterlogging Tolerance during the Seedling Stage in Maize 
Annals of Botany  2007;99(6):1067-1081.
Background and Aims
Soil waterlogging is a major environmental stress that suppresses maize (Zea mays) growth and yield. To identify quantitative trait loci (QTL) associated with waterlogging tolerance at the maize seedling stage, a F2 population consisting of 288 F2:3 lines was created from a cross between two maize genotypes, ‘HZ32’ (waterlogging-tolerant) and ‘K12’ (waterlogging-sensitive).
Methods
The F2 population was genotyped and a base-map of 1710·5 cM length was constructed with an average marker space of 11·5 cM based on 177 SSR (simple sequence repeat) markers. QTL associated with root length, root dry weight, plant height, shoot dry weight, total dry weight and waterlogging tolerance coefficient were identified via composite interval mapping (CIM) under waterlogging and control conditions in 2004 (EXP.1) and 2005 (EXP.2), respectively.
Key Results and Conclusions
Twenty-five and thirty-four QTL were detected in EXP.1 and EXP.2, respectively. The effects of each QTL were moderate, ranging from 3·9 to 37·3 %. Several major QTL determining shoot dry weight, root dry weight, total dry weight, plant height and their waterlogging tolerance coefficient each mapped on chromosomes 4 and 9. These QTL were detected consistently in both experiments. Secondary QTL influencing tolerance were also identified and located on chromosomes 1, 2, 3, 6, 7 and 10. These QTL were specific to particular traits or environments. Although the detected regions need to be mapped more precisely, the findings and QTL found in this study may provide useful information for marker-assisted selection (MAS) and further genetic studies on maize waterlogging tolerance.
doi:10.1093/aob/mcm055
PMCID: PMC3244372  PMID: 17470902
Maize (Zea mays); waterlogging tolerance; genome mapping; SSR marker; QTL; epistasis effect
4.  The Transcriptome of Brassica napus L. Roots under Waterlogging at the Seedling Stage 
Although rapeseed (Brassica napus L.) is known to be affected by waterlogging, the genetic basis of waterlogging tolerance by rapeseed is largely unknown. In this study, the transcriptome under 0 h and 12 h of waterlogging was assayed in the roots of ZS9, a tolerant variety, using digital gene expression (DGE). A total of 4432 differentially expressed genes were identified, indicating that the response to waterlogging in rapeseed is complicated. The assignments of the annotated genes based on GO (Gene Ontology) revealed there were more genes induced under waterlogging in “oxidation reduction”, “secondary metabolism”, “transcription regulation”, and “translation regulation”; suggesting these four pathways are enhanced under waterlogging. Analysis of the 200 most highly expressed genes illustrated that 144 under normal conditions were down-regulated by waterlogging, while up to 191 under waterlogging were those induced in response to stress. The expression of genes involved under waterlogging is mediated by multiple levels of transcriptional, post-transcriptional, translational and post-translational regulation, including phosphorylation and protein degradation; in particular, protein degradation might be involved in the negative regulation in response to this stress. Our results provide new insight into the response to waterlogging and will help to identify important candidate genes.
doi:10.3390/ijms14022637
PMCID: PMC3588007  PMID: 23358252
rapeseed (Brassica napus L.); waterlogging; DGE (digital gene expression); roots; transcriptome
5.  A Comparison of Screening Methods to Identify Waterlogging Tolerance in the Field in Brassica napus L. during Plant Ontogeny 
PLoS ONE  2014;9(3):e89731.
Waterlogging tolerance is typically evaluated at a specific development stage, with an implicit assumption that differences in waterlogging tolerance expressed in these systems will result in improved yield performance in fields. It is necessary to examine these criteria in fields.
In the present study, three experiments were conducted to screen waterlogging tolerance in 25 rapeseed (Brassica napus L.) varieties at different developmental stages, such as seedling establishment stage and seedling stage at controlled environment, and maturity stage in the fields. The assessments for physiological parameters at three growth stages suggest that there were difference of waterlogging tolerance at all the development stages, providing an important basis for further development of breeding more tolerant materials. The results indicated that flash waterlogging restricts plant growth and growth is still restored after removal of the stress. Correlation analysis between waterlogging tolerance coefficient (WTC) of yield and other traits revealed that there was consistency in waterlogging tolerance of the genotypes until maturity, and good tolerance at seedling establishment stage and seedling stage can guarantee tolerance in later stages. The waterlogging-tolerant plants could be selected using some specific traits at any stage, and selections would be more effective at the seedling establishment stage.
Thus, our study provides a method for screening waterlogging tolerance, which would enable the suitable basis for initial selection of a large number of germplasm or breeding populations for waterlogging tolerance and help for verifying their potential utility in crop-improvement.
doi:10.1371/journal.pone.0089731
PMCID: PMC3940661  PMID: 24594687
6.  Genome-Wide Expression of Transcriptomes and Their Co-Expression Pattern in Subtropical Maize (Zea mays L.) under Waterlogging Stress 
PLoS ONE  2013;8(8):e70433.
Waterlogging causes extensive damage to maize crops in tropical and subtropical regions. The identification of tolerance genes and their interactions at the molecular level will be helpful to engineer tolerant genotypes. A whole-genome transcriptome assay revealed the specific role of genes in response to waterlogging stress in susceptible and tolerant genotypes. Genes involved in the synthesis of ethylene and auxin, cell wall metabolism, activation of G-proteins and formation of aerenchyma and adventitious roots, were upregulated in the tolerant genotype. Many transcription factors, particularly ERFs, MYB, HSPs, MAPK, and LOB-domain protein were involved in regulation of these traits. Genes responsible for scavenging of ROS generated under stress were expressed along with those involved in carbohydrate metabolism. The physical locations of 21 genes expressed in the tolerant genotype were found to correspond with the marker intervals of known QTLs responsible for development of adaptive traits. Among the candidate genes, most showed synteny with genes of sorghum and foxtail millet. Co-expression analysis of 528 microarray samples including 16 samples from the present study generated seven functional modules each in the two genotypes, with differing characteristics. In the tolerant genotype, stress genes were co-expressed along with peroxidase and fermentation pathway genes.
doi:10.1371/journal.pone.0070433
PMCID: PMC3735631  PMID: 23936429
7.  Identification of QTLs for yield and yield components of barley under different growth conditions*  
Waterlogging is a major abiotic stress limiting barley (Hordeum vulgare L.) yield and its stability in areas with excessive rainfall. Identification of genomic regions influencing the response of yield and its components to waterlogging stress will enhance our understanding of the genetics of waterlogging tolerance and the development of more tolerant barley cultivars. Quantitative trait loci (QTLs) for grain yield and its components were identified using 156 doubled haploid (DH) lines derived from a cross between the cultivars Yerong (waterlogging-tolerant) and Franklin (waterlogging-sensitive) grown under different conditions (waterlogged and well drained). A total of 31 QTLs were identified for the measured characters from two experiments with two growth environments. The phenotypic variation explained by individual QTLs ranged from 4.74% to 55.34%. Several major QTLs determining kernel weight (KW), grains per spike (GS), spikes per plant (SP), spike length (SL) and grain yield (GY) were detected on the same region of chromosome 2H, indicating close linkage or pleiotropy of the gene(s) controlling these traits. Some different QTLs were identified under waterlogging conditions, and thus different markers may have to be used in selecting cultivars suitable for high rainfall areas.
doi:10.1631/jzus.B0900332
PMCID: PMC2833401  PMID: 20205303
Barley (Hordeum vulgare L.); Waterlogging tolerance; Yield; Quantitative trait locus (QTL)
8.  Waterlogging Tolerance of Crops: Breeding, Mechanism of Tolerance, Molecular Approaches, and Future Prospects 
BioMed Research International  2012;2013:963525.
Submergence or flood is one of the major harmful abiotic stresses in the low-lying countries and crop losses due to waterlogging are considerably high. Plant breeding techniques, conventional or genetic engineering, might be an effective and economic way of developing crops to grow successfully in waterlogged condition. Marker assisted selection (MAS) is a new and more effective approach which can identify genomic regions of crops under stress, which could not be done previously. The discovery of comprehensive molecular linkage maps enables us to do the pyramiding of desirable traits to improve in submergence tolerance through MAS. However, because of genetic and environmental interaction, too many genes encoding a trait, and using undesirable populations the mapping of QTL was hampered to ensure proper growth and yield under waterlogged conditions Steady advances in the field of genomics and proteomics over the years will be helpful to increase the breeding programs which will help to accomplish a significant progress in the field crop variety development and also improvement in near future. Waterlogging response of soybean and major cereal crops, as rice, wheat, barley, and maize and discovery of QTL related with tolerance of waterlogging, development of resistant variety, and, in addition, future prospects have also been discussed.
doi:10.1155/2013/963525
PMCID: PMC3591200  PMID: 23484164
9.  Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilisers during hypoxic stress 
Amino Acids  2010;39(4):1043-1053.
Alanine aminotransferase (AlaAT) catalyses the reversible conversion of pyruvate and glutamate into alanine and oxoglutarate. In soybean, two subclasses were identified, each represented by two highly similar members. To investigate the role of AlaAT during hypoxic stress in soybean, changes in transcript level of both subclasses were analysed together with the enzyme activity and alanine content of the tissue. Moreover, the dependency of AlaAT activity and gene expression was investigated in relation to the source of nitrogen supplied to the plants. Using semi-quantitative PCR, GmAlaAT genes were determined to be highest expressed in roots and nodules. Under normal growth conditions, enzyme activity of AlaAT was detected in all organs tested, with lowest activity in the roots. Upon waterlogging-induced hypoxia, AlaAT activity increased strongly. Concomitantly, alanine accumulated. During re-oxygenation, AlaAT activity remained high, but the transcript level and the alanine content decreased. Our results show a role for AlaAT in the catabolism of alanine during the initial period of re-oxygenation following hypoxia. GmAlaAT also responded to nitrogen availability in the solution during waterlogging. Ammonium as nitrogen source induced both gene expression and enzyme activity of AlaAT more than when nitrate was supplied in the nutrient solution. The work presented here indicates that AlaAT might not only be important during hypoxia, but also during the recovery phase after waterlogging, when oxygen is available to the tissue again.
doi:10.1007/s00726-010-0596-1
PMCID: PMC2945468  PMID: 20414691
Glycine max; Soybean; Alanine aminotransferase; Hypoxic stress; Waterlogging; Nitrogen fertilisation
10.  Conditional QTL mapping for waterlogging tolerance in two RILs populations of wheat 
SpringerPlus  2013;2:245.
Waterlogging is a widespread limiting factor for wheat production throughout the world, specially irrigated and high rainfall environments. Only few studies reported QTLs for waterlogging tolerance. To identify quantitative trait loci (QTLs) for waterlogging tolerance, root dry weight index (RDWI), shoot dry weight index (SDWI), total dry weight index (TDWI) were measured at seedling stage in two unrelated recombinant inbred lines (RILs) populations. These populations were International Triticeae Mapping Initiative (ITMI) population ‘W7984 / Opata85’, and ‘SHW-L1 × Chuanmai 32’ (SC) population. Conditional QTL mapping and unconditional QTL mapping were studied to dissect the genetic relationship between TDWI and its components of SDWI and TDWI. Total of 36 QTLs for waterlogging tolerance in ITMI population and 10 QTLs in SC population were identified in present study. Of them, 17 alleles from synthetic hexaploid wheat ‘W7984’ and 3 alleles from synthetic hexaploid wheat ‘SHW-L1’ contribute positively to waterlogging tolerance. Combinations of conditional and unconditional mapping methods indicate that SDWI showed tighter genetic correlation with TDWI than RDWI. This QTL identification study and dissection provide theoretical basis and application foundation to Marker-assisted selection (MAS) of waterlogging tolerance improvement in wheat.
doi:10.1186/2193-1801-2-245
PMCID: PMC3671099  PMID: 23750334
QTL; Waterlogging tolerance; Conditional and unconditional mapping
11.  Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions 
Journal of Experimental Botany  2013;65(1):261-273.
Ethylene-mediated reactive oxygen species signalling is involved in adaptive responses of wheat seedlings to waterlogged conditions through controlling formation of lysigenous aerenchyma and expression of genes encoding ethanol fermentation enzymes in roots
Exposing plants to hypoxic conditions greatly improves their anoxic stress tolerance by enhancing the activities of glycolysis and fermentation in roots. Ethylene may also be involved in these adaptive responses because its synthesis is increased in roots under hypoxic conditions. Here it is reported that pre-treatment of wheat seedlings with an ethylene precursor, 1-aminocyclopropanecarboxylic acid (ACC), enhanced accumulation of ethylene in the roots of wheat seedlings, and enhanced their tolerance of oxygen-deficient conditions through increasing the expression of genes encoding ethanol fermentation enzymes, alcohol dehydrogenase and pyruvate decarboxylase, in the roots. Lysigenous aerenchyma formation in root was induced by ACC pre-treatment and was further induced by growth under oxygen-deficient conditions. ACC pre-treatment increased the expression of three genes encoding respiratory burst oxidase homologue (a plant homologue of gp91phox in NADPH oxidase), which has a role in the generation of reactive oxygen species (ROS), in roots of seedlings. Co-treatment with ACC and an NADPH oxidase inhibitor, diphenyleneiodonium, partly suppressed the ACC-induced responses. These results suggest that ethylene and ROS are involved in adaptation of wheat seedlings to oxygen-deficient conditions through controlling lysigenous aerenchyma formation and the expression of genes encoding ethanol fermentation enzymes.
doi:10.1093/jxb/ert371
PMCID: PMC3883296  PMID: 24253196
Aerenchyma; ethylene; fermentation; oxygen deficiency; reactive oxygen species; wheat (Triticum aestivum L.).
12.  Review of wheat improvement for waterlogging tolerance in Australia and India: the importance of anaerobiosis and element toxicities associated with different soils 
Annals of Botany  2008;103(2):221-235.
Background and Aims
The lack of knowledge about key traits in field environments is a major constraint to germplasm improvement and crop management because waterlogging-prone environments are highly diverse and complex, and the mechanisms of tolerance to waterlogging include a large range of traits. A model is proposed that waterlogging tolerance is a product of tolerance to anaerobiosis and high microelement concentrations. This is further evaluated with the aim of prioritizing traits required for waterlogging tolerance of wheat in the field.
Methods
Waterlogging tolerance mechanisms of wheat are evaluated in a range of diverse environments through a review of past research in Australia and India; this includes selected soils and plant data, including plant growth under waterlogged and drained conditions in different environments. Measurements focus on changes in redox potential and concentrations of diverse elements in soils and plants during waterlogging.
Key Results
(a) Waterlogging tolerance of wheat in one location often does not relate to another, and (b) element toxicities are often a major constraint in waterlogged environments. Important element toxicities in different soils during waterlogging include Mn, Fe, Na, Al and B. This is the first time that Al and B toxicities have been indicated for wheat in waterlogged soils in India. These results support and extend the well-known interactions of salinity/Na and waterlogging/hypoxia tolerance.
Conclusions
Diverse element toxicities (or deficiencies) that are exacerbated during waterlogging are proposed as a major reason why waterlogging tolerance at one site is often not replicated at another. Recommendations for germplasm improvement for waterlogging tolerance include use of inductively coupled plasma analyses of soils and plants.
doi:10.1093/aob/mcn137
PMCID: PMC2707304  PMID: 18708642
Waterlogging; microelements; toxicity; redox potential; wheat; anaerobiosis
13.  Subtractive hybridization-mediated analysis of genes and in silico prediction of associated microRNAs under waterlogged conditions in sugarcane (Saccharum spp.) 
FEBS Open Bio  2014;4:533-541.
Highlights
•Waterlogging adversely affects sugarcane productivity and quality.•A subtractive cDNA library was prepared from sugarcane leaf tissue and sequenced to generate ESTs.•EST sequences were used to identify transcripts induced by waterlogging.•The sequenced clones were classified by predicted functions and stress-related genes formed the largest class.•EST sequences were also used to identify putative novel microRNAs and their targets.
Sugarcane is an important tropical cash crop meeting 75% of world sugar demand and it is fast becoming an energy crop for the production of bio-fuel ethanol. A considerable area under sugarcane is prone to waterlogging which adversely affects both cane productivity and quality. In an effort to elucidate the genes underlying plant responses to waterlogging, a subtractive cDNA library was prepared from leaf tissue. cDNA clones were sequenced and annotated for their putative functions. Major groups of ESTs were related to stress (15%), catalytic activity (13%), cell growth (10%) and transport related proteins (6%). A few stress-related genes were identified, including senescence-associated protein, dehydration-responsive family protein, and heat shock cognate 70 kDa protein. A bioinformatics search was carried out to discover novel microRNAs (miRNAs) that can be regulated in sugarcane plants subjected to waterlogging stress. Taking advantage of the presence of miRNA precursors in the related sorghum genome, seven candidate mature miRNAs were identified in sugarcane. The application of subtraction technology allowed the identification of differentially expressed sequences and novel miRNAs in sugarcane under waterlogging stress. The comparative global transcript profiling in sugarcane plants undertaken in this study suggests that proteins associated with stress response, signal transduction, metabolic activity and ion transport play important role in conferring waterlogging tolerance in sugarcane.
doi:10.1016/j.fob.2014.05.007
PMCID: PMC4087145
ABA, abscisic acid; ADF, actin depolymerizing factor; ESTs, expressed sequence tags; Hsps, heat shock proteins; PTGS, post-transcriptional gene silencing; REMs, remorins; SSA, snow pea pod senescence-associated; SUCEST, sugarcane EST database; TGS, transcriptional gene silencing; EST; Novel miRNAs; Sugarcane; Suppression subtractive hybridization; Waterlogging stress
14.  From epoxycarotenoids to ABA: the role of ABA 8′-hydroxylases in drought-stressed maize roots 
The ability of plants to withstand drought, a potentially major constraint to yield and production, is influenced by abscisic acid (ABA). ABA is synthesized in the cytosol from plastid carotenoid pathway derived precursors, and later inactivated by the action of ABA hydroxylases. Endogenous accumulation of ABA is controlled by both its synthesis and catabolism. Enzymatic activity of ABA 8′-hydroxylase (ABA8Ox), also referred to as CYP707A, is considered one of the key steps in modulating ABA levels that control numerous physiological processes. To investigate the role of this enzyme, maize ABA8Ox gene family members were identified. ABA8Ox gene expression was then analyzed in different tissues and roots during the drought-stress response in maize. These genes were found to be expressed in all tissues, with a high degree of specificity to each tissue and some degree of overlap. Maize ABA8Ox1a and ABA8Ox1b were shown to be the major transcript components for regulating ABA catabolism in drought-stressed roots. Phylogenetic and gene-structure analyses were performed to extend the implications and infer the cause of ABA catabolism in other cereal crops.
doi:10.1016/j.abb.2010.07.005
PMCID: PMC2957537  PMID: 20637177
ABA; abiotic stress; carotenoids; maize; sorghum; rice
15.  Characterization of miRNAs in Response to Short-Term Waterlogging in Three Inbred Lines of Zea mays 
PLoS ONE  2012;7(6):e39786.
Waterlogging of plants leads to low oxygen levels (hypoxia) in the roots and causes a metabolic switch from aerobic respiration to anaerobic fermentation that results in rapid changes in gene transcription and protein synthesis. Our research seeks to characterize the microRNA-mediated gene regulatory networks associated with short-term waterlogging. MicroRNAs (miRNAs) are small non-coding RNAs that regulate many genes involved in growth, development and various biotic and abiotic stress responses. To characterize the involvement of miRNAs and their targets in response to short-term hypoxia conditions, a quantitative real time PCR (qRT-PCR) assay was used to quantify the expression of the 24 candidate mature miRNA signatures (22 known and 2 novel mature miRNAs, representing 66 miRNA loci) and their 92 predicted targets in three inbred Zea mays lines (waterlogging tolerant Hz32, mid-tolerant B73, and sensitive Mo17). Based on our studies, miR159, miR164, miR167, miR393, miR408 and miR528, which are mainly involved in root development and stress responses, were found to be key regulators in the post-transcriptional regulatory mechanisms under short-term waterlogging conditions in three inbred lines. Further, computational approaches were used to predict the stress and development related cis-regulatory elements on the promoters of these miRNAs; and a probable miRNA-mediated gene regulatory network in response to short-term waterlogging stress was constructed. The differential expression patterns of miRNAs and their targets in these three inbred lines suggest that the miRNAs are active participants in the signal transduction at the early stage of hypoxia conditions via a gene regulatory network; and crosstalk occurs between different biochemical pathways.
doi:10.1371/journal.pone.0039786
PMCID: PMC3387268  PMID: 22768123
16.  A Single Locus Is Responsible for Salinity Tolerance in a Chinese Landrace Barley (Hordeum vulgare L.) 
PLoS ONE  2012;7(8):e43079.
Introduction
Salinity and waterlogging are two major abiotic stresses severely limiting barley production. The lack of a reliable screening method makes it very hard to improve the tolerance through breeding programs.
Methods
This work used 188 DH lines from a cross between a Chinese landrace variety, TX9425 (waterlogging and salinity tolerant), and a Japanese malting barley, Naso Nijo (waterlogging and salinity sensitive), to identify QTLs associated with the tolerance.
Results
Four QTLs were found for waterlogging tolerance. The salinity tolerance was evaluated with both a hydroponic system and in potting mixture. In the trial with potting mixture, only one major QTL was identified to associate with salinity tolerance. This QTL explained nearly 50% of the phenotypic variation, which makes it possible for further fine mapping and cloning of the gene. This QTL was also identified in the hydroponic experiment for different salt-related traits. The position of this QTL was located at a similar position to one of the major QTLs for waterlogging tolerance, indicating the possibility of similar mechanisms controlling both waterlogging and salinity tolerance.
Conclusion
The markers associated with the QTL provided a unique opportunity in breeding programs for selection of salinity and waterlogging tolerance.
doi:10.1371/journal.pone.0043079
PMCID: PMC3423432  PMID: 22916210
17.  G proteins as regulators in ethylene-mediated hypoxia signaling 
Plant Signaling & Behavior  2010;5(4):375-378.
Waterlogging or flooding are frequently or constitutively encountered by many plant species. The resulting reduction in endogenous O2 concentration poses a severe threat. Numerous adaptations at the anatomical, morphological and metabolic level help plants to either escape low oxygen conditions or to endure them. Formation of aerenchyma or rapid shoot elongation are escape responses, as is the formation of adventitious roots. The metabolic shift from aerobic respiration to anaerobic fermentation contributes to a basal energy supply at low oxygen conditions. Ethylene plays a central role in hypoxic stress signaling, and G proteins have been recognized as crucial signal transducers in various hypoxic signaling pathways. The programmed death of parenchyma cells that results in hypoxia-induced aerenchyma formation is an ethylene response. In maize, aerenchyma are induced in the absence of ethylene when G proteins are constitutively activated. Similarly, ethylene induced death of epidermal cells that cover adventitious roots at the stem node of rice is strictly dependent on heterotrimeric G protein activity. Knock down of the unique Gα gene RGA1 in rice prevents epidermal cell death. Finally, in Arabidopsis, induction of alcohol dehydrogenase with resulting increased plant survival relies on the balanced activities of a small Rop G protein and its deactivating protein RopGAP4. Identifying the general mechanisms of G protein signaling in hypoxia adaptation of plants is one of the tasks ahead.
PMCID: PMC2958587  PMID: 20948297
submergence; hypoxia; ethylene; G protein; reactive oxygen species; H2O2
18.  Comparisons of early transcriptome responses to low-oxygen environments in three dicotyledonous plant species 
Plant Signaling & Behavior  2010;5(8):1006-1009.
Waterlogging is a serious impediment to crop productivity worldwide which acts to reduce oxygen levels in the rhizosphere due to the low diffusion rate of molecular oxygen in water. Plants respond to low oxygen through rapid and specific changes at both the transcriptional and translational levels. Transcriptional changes to low-oxygen (hypoxia) stress have been studied in a number of plant species using whole genome microarrays. Using transcriptome data from root tissue from early time points (4–5 h) from cotton (Gossypium hirsutum), Arabidopsis and gray poplar (Populus x canescens), we have identified a core set of orthologous genes that responded to hypoxia in similar ways between species, and others that showed species specific responses. Responses to hypoxia were most similar between Arabidopsis and cotton, while the waterlogging tolerant poplar species exhibited some significant differences.
doi:10.4161/psb.5.8.12231
PMCID: PMC3115181  PMID: 20724824
low-oxygen stress; hypoxia; abiotic stress; waterlogging; Arabidopsis thaliana; Gossypium hirsutum; cotton; Populus x canescens; gray poplar
19.  The R2R3-MYB Transcription Factor Gene Family in Maize 
PLoS ONE  2012;7(6):e37463.
MYB proteins comprise a large family of plant transcription factors, members of which perform a variety of functions in plant biological processes. To date, no genome-wide characterization of this gene family has been conducted in maize (Zea mays). In the present study, we performed a comprehensive computational analysis, to yield a complete overview of the R2R3-MYB gene family in maize, including the phylogeny, expression patterns, and also its structural and functional characteristics. The MYB gene structure in maize and Arabidopsis were highly conserved, indicating that they were originally compact in size. Subgroup-specific conserved motifs outside the MYB domain may reflect functional conservation. The genome distribution strongly supports the hypothesis that segmental and tandem duplication contribute to the expansion of maize MYB genes. We also performed an updated and comprehensive classification of the R2R3-MYB gene families in maize and other plant species. The result revealed that the functions were conserved between maize MYB genes and their putative orthologs, demonstrating the origin and evolutionary diversification of plant MYB genes. Species-specific groups/subgroups may evolve or be lost during evolution, resulting in functional divergence. Expression profile study indicated that maize R2R3-MYB genes exhibit a variety of expression patterns, suggesting diverse functions. Furthermore, computational prediction potential targets of maize microRNAs (miRNAs) revealed that miR159, miR319, and miR160 may be implicated in regulating maize R2R3-MYB genes, suggesting roles of these miRNAs in post-transcriptional regulation and transcription networks. Our comparative analysis of R2R3-MYB genes in maize confirm and extend the sequence and functional characteristics of this gene family, and will facilitate future functional analysis of the MYB gene family in maize.
doi:10.1371/journal.pone.0037463
PMCID: PMC3370817  PMID: 22719841
20.  Exploring the maize rhizosphere microbiome in the field 
Maize is one of the most economically important crops in the world. Understanding how the genetics and management of this staple crop interact with local field environments is vital to securing sustainable harvests. The interface zone between the plant root and its surrounding soil, or rhizosphere, supports essential interactions between roots and local soils. These interactions include the exchange of carbon for nutrients and are strongly influenced by the microbial constituents of the soil, or the microbiome. In a recent multi-environment study, we explored the diversity and heritability of the maize rhizosphere microbiome at flowering time. We assessed the bacterial diversity of the maize rhizosphere by pyrosequencing of 16S rRNA genes obtained from soil surrounding the roots of 27 genetically diverse maize inbreds grown in five field environments. We then partitioned variation in α- and β-diversity of the microbiome across plant inbreds in the different fields. The results of this study revealed the heritability and significance of genotype-by-environment interactions on the maize rhizosphere microbiome at a single time point. Longitudinal studies detailing the maize rhizosphere throughout an entire growing season are currently underway and should provide a more detailed view of how plant genotypes interact with the environment to shape the microbiome. Future efforts will aim to incorporate these interactions into genetic models of economically important traits such as yield.
doi:10.4161/cib.25177
PMCID: PMC3829924  PMID: 24265851
maize; rhizosphere; microbiome; GxE; 16S rRNA; heritability
21.  Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants 
Nature  2011;479(7373):415-418.
Plants and animals are obligate aerobes, requiring oxygen for mitochondrial respiration and energy production. In plants, an unanticipated decline in oxygen availability (hypoxia), as caused by root waterlogging or foliage submergence, triggers changes in gene transcription and mRNA translation that promote anaerobic metabolism and thus sustain substrate-level ATP production1. In contrast to animals2, oxygen sensing has not been ascribed to a mechanism of gene regulation in response to oxygen deprivation in plants. Here we show that the N-end rule pathway of targeted proteolysis acts as a homeostatic sensor of severe low oxygen in Arabidopsis, through its regulation of key hypoxia response transcription factors. We found that plants lacking components of the N-end rule pathway constitutively express core hypoxia response genes and are more tolerant of hypoxic stress. We identify the hypoxia-associated Ethylene Response Factor (ERF) Group VII transcription factors of Arabidopsis as substrates of this pathway. Regulation of these proteins by the N-end rule pathway occurs through a characteristic conserved motif at the N-terminus initiating with MetCys- (MC-). Enhanced stability of one of these proteins, HRE2, under low oxygen conditions improves hypoxia survival and reveals a molecular mechanism for oxygen sensing in plants via the evolutionarily conserved N-end rule pathway. SUB1A-1, a major determinant of submergence tolerance in rice3, was shown not to be a substrate for the N-end rule pathway despite containing the N-terminal motif, suggesting that it is uncoupled from N-end rule pathway regulation, and that enhanced stability may relate to the superior tolerance of Sub1 rice varieties to multiple abiotic stresses4.
doi:10.1038/nature10534
PMCID: PMC3223408  PMID: 22020279
22.  Tissue localization of maize acetylcholinesterase associated with heat tolerance in plants 
Plant Signaling & Behavior  2012;7(3):301-305.
Our recent study reported that maize acetylcholinesterase (AChE) activity in the coleoptile node is enhanced through a post-translational modification response to heat stress and transgenic plants overexpressing maize AChE gene had an elevated heat tolerance, which strongly suggests that maize AChE plays a positive, important role in maize heat tolerance. Here we present (1) maize AChE activity in the mesocotyl also enhances during heat stress and (2) maize AChE mainly localizes in vascular bundles including endodermis and epidermis in coleoptile nodes and mesocotyls of maize seedlings.
doi:10.4161/psb.19007
PMCID: PMC3443906  PMID: 22476469
acetylcholine; acetylcholinesterase; heat stress; maize; plant neurobiology
23.  Alternative 5' splice site selection induced by heat shock. 
Molecular and Cellular Biology  1994;14(1):567-575.
The mouse HSP47 gene consists of six exons separated by five introns. Three HSP47 cDNAs differing only in their 5' noncoding regions have been reported. One of these alternatively spliced mRNAs was detected only after heat shock, which caused an alternative 5' splice donor site selection. Other stress inducers, including an amino acid analog and sodium arsenite, had no effect on the alternative splicing. The alternatively spliced mRNA, which was 169 nucleotides longer in the 5' noncoding region compared to mRNA transcribed in non-heat shock conditions, was efficiently translated under heat shock conditions. This novel finding that alternative splicing is caused by artificial treatment like heat shock will provide a useful in vivo model for understanding the exon-intron recognition mechanism as well as heat shock-induced alterations in gene expression.
Images
PMCID: PMC358406  PMID: 8264624
24.  The cardiac troponin T alternative exon contains a novel purine-rich positive splicing element. 
Molecular and Cellular Biology  1993;13(6):3660-3674.
We have characterized a novel positive-acting splicing element within the developmentally regulated alternative exon (exon 5) of the cardiac troponin T (cTNT) gene. The exon splicing element (ESE) is internal to the exon portions of the splice sites and is required for splicing to the 3' splice site but not the 5' splice site flanking the exon. Sequence comparisons between cTNT exon 5 and other exons that contain regions required for splicing reveal a common purine-rich motif. Sequence within cTNT exon 5 or a synthetic purine-rich motif facilitates splicing of heterologous alternative and constitutive splice sites in vivo. Interestingly, the ESE is not required for the preferential inclusion of cTNT exon 5 observed in primary skeletal muscle cultures. Our results strongly suggest that the purine-rich ESE serves as a general splicing element that is recognized by the constitutive splicing machinery.
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PMCID: PMC359835  PMID: 8388541
25.  Seed priming with chitosan improves maize germination and seedling growth in relation to physiological changes under low temperature stress*  
Low temperature stress during germination and early seedling growth is an important constraint of global production of maize. The effects of seed priming with 0.25%, 0.50%, and 0.75% (w/v) chitosan solutions at 15 °C on the growth and physiological changes were investigated using two maize (Zea mays L.) inbred lines, HuangC (chilling-tolerant) and Mo17 (chilling-sensitive). While seed priming with chitosan had no significant effect on germination percentage under low temperature stress, it enhanced germination index, reduced the mean germination time (MGT), and increased shoot height, root length, and shoot and root dry weights in both maize lines. The decline of malondialdehyde (MDA) content and relative permeability of the plasma membrane and the increase of the concentrations of soluble sugars and proline, peroxidase (POD) activity, and catalase (CAT) activity were detected both in the chilling-sensitive and chilling-tolerant maize seedlings after priming with the three concentrations of chitosan. HuangC was less sensitive to responding to different concentrations of chitosan. Priming with 0.50% chitosan for about 60~64 h seemed to have the best effects. Thus, it suggests that seed priming with chitosan may improve the speed of germination of maize seed and benefit for seedling growth under low temperature stress.
doi:10.1631/jzus.B0820373
PMCID: PMC2689555  PMID: 19489108
Seed priming; Chitosan; Low temperature stress; Germination; Physiological changes; Maize

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