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1.  Biomass Enzymatic Saccharification Is Determined by the Non-KOH-Extractable Wall Polymer Features That Predominately Affect Cellulose Crystallinity in Corn 
PLoS ONE  2014;9(9):e108449.
Corn is a major food crop with enormous biomass residues for biofuel production. Due to cell wall recalcitrance, it becomes essential to identify the key factors of lignocellulose on biomass saccharification. In this study, we examined total 40 corn accessions that displayed a diverse cell wall composition. Correlation analysis showed that cellulose and lignin levels negatively affected biomass digestibility after NaOH pretreatments at p<0.05 & 0.01, but hemicelluloses did not show any significant impact on hexoses yields. Comparative analysis of five standard pairs of corn samples indicated that cellulose and lignin should not be the major factors on biomass saccharification after pretreatments with NaOH and H2SO4 at three concentrations. Notably, despite that the non-KOH-extractable residues covered 12%–23% hemicelluloses and lignin of total biomass, their wall polymer features exhibited the predominant effects on biomass enzymatic hydrolysis including Ara substitution degree of xylan (reverse Xyl/Ara) and S/G ratio of lignin. Furthermore, the non-KOH-extractable polymer features could significantly affect lignocellulose crystallinity at p<0.05, leading to a high biomass digestibility. Hence, this study could suggest an optimal approach for genetic modification of plant cell walls in bioenergy corn.
PMCID: PMC4177209  PMID: 25251456
2.  Genome-Wide Identification, Evolution and Expression Analysis of mTERF Gene Family in Maize 
PLoS ONE  2014;9(4):e94126.
Plant mitochondrial transcription termination factor (mTERF) genes comprise a large family with important roles in regulating organelle gene expression. In this study, a comprehensive database search yielded 31 potential mTERF genes in maize (Zea mays L.) and most of them were targeted to mitochondria or chloroplasts. Maize mTERF were divided into nine main groups based on phylogenetic analysis, and group IX represented the mitochondria and species-specific clade that diverged from other groups. Tandem and segmental duplication both contributed to the expansion of the mTERF gene family in the maize genome. Comprehensive expression analysis of these genes, using microarray data and RNA-seq data, revealed that these genes exhibit a variety of expression patterns. Environmental stimulus experiments revealed differential up or down-regulation expression of maize mTERF genes in seedlings exposed to light/dark, salts and plant hormones, respectively, suggesting various important roles of maize mTERF genes in light acclimation and stress-related responses. These results will be useful for elucidating the roles of mTERF genes in the growth, development and stress response of maize.
PMCID: PMC3981765  PMID: 24718683
3.  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.
PMCID: PMC3828346  PMID: 24244474
4.  Fine Mapping and Candidate Gene Prediction of a Pleiotropic Quantitative Trait Locus for Yield-Related Trait in Zea mays 
PLoS ONE  2012;7(11):e49836.
The yield of maize grain is a highly complex quantitative trait that is controlled by multiple quantitative trait loci (QTLs) with small effects, and is frequently influenced by multiple genetic and environmental factors. Thus, it is challenging to clone a QTL for grain yield in the maize genome. Previously, we identified a major QTL, qKNPR6, for kernel number per row (KNPR) across multiple environments, and developed two nearly isogenic lines, SL57-6 and Ye478, which differ only in the allelic constitution at the short segment harboring the QTL. Recently, qKNPR6 was re-evaluated in segregating populations derived from SL57-6×Ye478, and was narrowed down to a 2.8 cM interval, which explained 56.3% of the phenotypic variance of KNPR in 201 F2∶3 families. The QTL simultaneously affected ear length, kernel weight and grain yield. Furthermore, a large F2 population with more than 12,800 plants, 191 recombinant chromosomes and 10 overlapping recombinant lines placed qKNPR6 into a 0.91 cM interval corresponding to 198Kb of the B73 reference genome. In this region, six genes with expressed sequence tag (EST) evidence were annotated. The expression pattern and DNA diversity of the six genes were assayed in Ye478 and SL57-6. The possible candidate gene and the pathway involved in inflorescence development were discussed.
PMCID: PMC3504098  PMID: 23185451
5.  Prolyl 4-hydroxylase genes are subjected to alternative splicing in roots of maize seedlings under waterlogging 
Annals of Botany  2011;108(7):1323-1335.
In animals, prolyl 4-hydroxylases (P4Hs) are regarded as oxygen sensors under hypoxia stress, but little is known about their role in the response to waterlogging in maize.
A comprehensive genome-wide analysis of P4H genes of maize (zmP4H genes) was carried out, including gene structures, phylogeny, protein motifs, chromosomal locations and expression patterns under waterlogging.
Key Results
Nine zmP4H genes were identified in maize, of which five were alternatively spliced into at least 19 transcripts. Different alternative splicing (AS) events were revealed in different inbred lines, even for the same gene, possibly because of organ and developmental specificities or different stresses. The signal strength of splice sites was strongly correlated with selection of donor and receptor sites, and ambiguous junction sites due to small direct repeats at the exon/intron junction frequently resulted in the selection of unconventional splicing sites. Eleven out of 14 transcripts resulting from AS harboured a premature termination codon, rendering them potential candidates for nonsense-mediated RNA degradation. Reverse transcription–PCR (RT–PCR) indicated that zmP4H genes displayed different expression patterns under waterlogging. The diverse transcripts generated from AS were expressed at different levels, suggesting that zmP4H genes were under specific control by post-transcriptional regulation under waterlogging stress in the line HZ32.
Our results provide a framework for future dissection of the function of the emerging zmP4H family and suggest that AS might have an important role in the regulation of the expression profile of this gene family under waterlogging stress.
PMCID: PMC3197451  PMID: 21969257
Maize; Zea mays; prolyl 4-hydroxylase; zmP4H; alternative splicing; AS; waterlogging; flooding stress
6.  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.
PMCID: PMC3387268  PMID: 22768123
7.  Identification of transcriptome induced in roots of maize seedlings at the late stage of waterlogging 
BMC Plant Biology  2010;10:189.
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.
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.
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.
PMCID: PMC2956539  PMID: 20738849
8.  Differential expression of miRNAs in response to salt stress in maize roots 
Annals of Botany  2008;103(1):29-38.
Background and Aims
Corn (Zea mays) responds to salt stress via changes in gene expression, metabolism and physiology. This adaptation is achieved through the regulation of gene expression at the transcriptional and post-transcriptional levels. MicroRNAs (miRNAs) have been found to act as key regulating factors of post-transcriptional gene expression. However, little is known about the role of miRNAs in plants' responses to abiotic stresses.
A custom μparaflo™ microfluidic array containing release version 10.1 plant miRNA probes ( was used to discover salt stress-responsive miRNAs using the differences in miRNA expression between the salt-tolerant maize inbred line ‘NC286’ and the salt-sensitive maize line ‘Huangzao4’.
Key Results
miRNA microarray hybridization revealed that a total of 98 miRNAs, from 27 plant miRNA families, had significantly altered expression after salt treatment. These miRNAs displayed different activities in the salt response, and miRNAs belonging to the same miRNA family showed the same behaviour. Interestingly, 18 miRNAs were found which were only expressed in the salt-tolerant maize line, and 25 miRNAs that showed a delayed regulation pattern in the salt-sensitive line. A gene model was proposed that showed how miRNAs could regulate the abiotic stress-associated process and the gene networks coping with the stress.
Salt-responsive miRNAs are involved in the regulation of metabolic, morphological and physiological adaptations of maize seedlings at the post-transcriptional level. The miRNA genotype-specific expression model might explain the distinct salt sensitivities between maize lines.
PMCID: PMC2707283  PMID: 18952624
Salt stress; Zea mays; microRNA; microarray; transcription regulation; Zea mays
9.  Submergence-responsive MicroRNAs are Potentially Involved in the Regulation of Morphological and Metabolic Adaptations in Maize Root Cells 
Annals of Botany  2008;102(4):509-519.
Background and Aims
Anaerobic or low oxygen conditions occur when maize plants are submerged or subjected to flooding of the soil. Maize survival under low oxygen conditions is largely dependent on metabolic, physiological and morphological adaptation strategies; the regulation mechanisms of which remain unknown. MicroRNAs (miRNAs) play critical roles in the response to adverse biotic or abiotic stresses at the post-transcriptional level. The aim of this study was to understand submergence-responsive miRNAs and their potential roles in submerged maize roots.
A custom μParaflo™ microfluidic array containing plant miRNA (miRBase: probes was used to explore differentially expressed miRNAs. Small RNAs from treated roots were hybridized with the microarray. The targets and their cis-acting elements of small RNA were predicted and analysed by RT-PCR.
Key Results
Microarray data revealed that the expression levels of 39 miRNAs from nine maize and some other plant miRNA families were significantly altered (P < 0·01). Four expression profiles were identified across different submergence time-points. The zma-miRNA166, zma-miRNA167, zma-miRNA171 and osa-miRNA396-like were induced in the early phase, and their target genes were predicted to encode important transcription factors, including; HD-ZIP, auxin response factor, SCL and the WRKY domain protein. zma-miR159, ath-miR395-like, ptc-miR474-like and osa-miR528-like were reduced at the early submergence phase and induced after 24 h of submergence. The predicted targets for these miRNAs were involved in carbohydrate and energy metabolism, including starch synthase, invertase, malic enzyme and ATPase. In addition, many of the predicted targets were involved in the elimination of reactive oxygen species and acetaldehyde. Overall, most of the targets of induced miRNAs contained the cis-acting element, which is essential for the anaerobic response or hormone induction.
Submergence-responsive miRNAs are involved in the regulation of metabolic, physiological and morphological adaptations of maize roots at the post-transcriptional level.
PMCID: PMC2701776  PMID: 18669574
Anaerobic metabolism; Zea mays; gene expression; transcription factor; microRNA; flooding stress
10.  Transcriptional and post-transcriptional regulation of gene expression in submerged root cells of maize 
Plant Signaling & Behavior  2009;4(2):132-135.
Maize survival under the anaerobic stress due to submergence conditions is dependent on complex metabolic, physiological and morphological adaptation strategies. Here, we focus on gene expression regulation at the transcriptional and post-transcriptional level in submerged maize root cells. Early in progressive oxygen deprivation, root cells sense the low oxygen signal to trigger expressions of TF genes, anaerobic response genes and miRNA genes. The induced TFs, in turn, promote a broad spectrum of responses from morphogenetic to metabolic; these responses occur at later stages of the stress treatment. The selective translation of anaerobically induced transcripts and selective degradation of some APs are also suggested to be an important regulatory mechanism. In addition, miRNAs are possibly transcriptionally regulated in submerged root cells and involved in post-transcriptional control of target genes. Thus, regulation of gene expression in response to low oxygen involves in significant transcriptional and post-transcriptional control.
PMCID: PMC2637500  PMID: 19649190
maize; Zea mays L.; anaerobic stress; adaptation; gene expression; microRNA
11.  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).
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.
PMCID: PMC3244372  PMID: 17470902
Maize (Zea mays); waterlogging tolerance; genome mapping; SSR marker; QTL; epistasis effect

Results 1-11 (11)