Effects Of Drought On Gene Expression In Maize Reproductive And Leaf Meristem Tissue Revealed By RNA-Seq1[W][OA]
Akshay Kakumanu, Madana M. R. Ambavaram, Curtis Klumas, A. Krishnan, Utlwang Batlang, Elijah Myers, Ruth Grene, A. Pereira
Published 2012 · Biology, Medicine
Download PDFAnalyze on Scholarcy
Drought stress affects cereals especially during the reproductive stage. The maize (Zea mays) drought transcriptome was studied using RNA-Seq analysis to compare drought-treated and well-watered fertilized ovary and basal leaf meristem tissue. More drought-responsive genes responded in the ovary compared with the leaf meristem. Gene Ontology enrichment analysis revealed a massive decrease in transcript abundance of cell division and cell cycle genes in the drought-stressed ovary only. Among Gene Ontology categories related to carbohydrate metabolism, changes in starch and Suc metabolism-related genes occurred in the ovary, consistent with a decrease in starch levels, and in Suc transporter function, with no comparable changes occurring in the leaf meristem. Abscisic acid (ABA)-related processes responded positively, but only in the ovaries. Related responses suggested the operation of low glucose sensing in drought-stressed ovaries. The data are discussed in the context of the susceptibility of maize kernel to drought stress leading to embryo abortion and the relative robustness of dividing vegetative tissue taken at the same time from the same plant subjected to the same conditions. Our working hypothesis involves signaling events associated with increased ABA levels, decreased glucose levels, disruption of ABA/sugar signaling, activation of programmed cell death/senescence through repression of a phospholipase C-mediated signaling pathway, and arrest of the cell cycle in the stressed ovary at 1 d after pollination. Increased invertase levels in the stressed leaf meristem, on the other hand, resulted in that tissue maintaining hexose levels at an “unstressed” level, and at lower ABA levels, which was correlated with successful resistance to drought stress.
This paper references
ADP-Glucose Pyrophosphorylase-Deficient Pea Embryos Reveal Specific Transcriptional and Metabolic Changes of Carbon-Nitrogen Metabolism and Stress Responses1[W]
K. Weigelt (2008)
The Arabidopsis bZIP Gene AtbZIP63 Is a Sensitive Integrator of Transient Abscisic Acid and Glucose Signals1[W][OA]
C. Matiolli (2011)
Function and regulation of phospholipid signalling in plants
H. Xue (2009)
AGPase knockdown pea
Abscisic acid: emergence of a core signaling network.
S. Cutler (2010)
Comparing regional transcript profiles from maize primary roots under well-watered and low water potential conditions.
V. Poroyko (2007)
Extranuclear protection of chromosomal DNA from oxidative stress
Sandy Vanderauwera (2011)
Control of Abscisic Acid Catabolism and Abscisic Acid Homeostasis Is Important for Reproductive Stage Stress Tolerance in Cereals1[W][OA]
Xuemei Ji (2011)
Understanding Oxidative Stress and Antioxidant Functions to Enhance Photosynthesis1
C. Foyer (2010)
Drought stress and reactive oxygen species: Production, scavenging and signaling.
Cruz de Carvalho Mh (2008)
A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize.
B. Usadel (2009)
Invertase cell wall4, mRNA
A central integrator of transcription networks in plant stress and energy signalling
E. Baena-González (2007)
The developmental context of cell-cycle control in plants.
S. D. de Jager (2005)
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments
G. Smyth (2004)
Relationship of carbohydrate and abscisic acid levels to kernel set in maize under postpollination water deficit.
T. Setter (2010)
Ribonucleotide Reductase Regulation in Response to Genotoxic Stress in Arabidopsis1[W]
Hélène Roa (2009)
Synergistic influence of sucrose and abscisic acid on the genes involved in starch synthesis in maize endosperm.
J. Chen (2011)
Quantitative analysis of cell division in leaves: methods, developmental patterns and effects of environmental conditions
F. Tardieu (2004)
Transpiration- and growth-induced water potentials in maize.
M. Westgate (1984)
The increased expression of the genes involved in ABA synthesis and the ABI5 transcription factor in the drought-stressed ovary tissue
Characterization of dull1, a Maize Gene Coding for a Novel Starch Synthase
M. Gao (1998)
A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana.
L. Lopez-Molina (2000)
The role of phospholipase D in plant stress responses.
Bastiaan O. R. Bargmann (2006)
Arabidopsis mutants simulating disease resistance response
R. Dietrich (1994)
Drought stress and reactive oxygen species: Production, scavenging and signaling.
M. H. Cruz de Carvalho (2008)
Roles of carbohydrate supply and ethylene, polyamines in maize kernel set.
Han-Yu Feng (2011)
Use of expression analysis to dissect alterations in carbohydrate metabolism in wheat leaves during drought stress
G. Xue (2008)
Sugar perception and signaling--an update.
J. Hanson (2009)
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.
C. Trapnell (2010)
Characterization of SSIIIadeficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm
N Fujita (2007)
The developmental dynamics of the maize leaf transcriptome
P. Li (2010)
MYB transcription factors in Arabidopsis.
C. Dubos (2010)
Functional reversion to identify controlling genes in multigenic responses: analysis of floral abortion.
John S. Boyer (2007)
A direct approach to false discovery rates
John D. Storey (2002)
Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity.
Yueyun Hong (2010)
Bax inhibitor-1: a highly conserved endoplasmic reticulum-resident cell death suppressor
T. Ishikawa (2011)
Regulatory Functions of Nuclear Hexokinase1 Complex in Glucose Signaling
Young-Hee Cho (2006)
Nuf2, a spindle pole body-associated protein required for nuclear division in yeast
M. A. Osborne (1994)
The gene encoding starch synthase IIc exists in maize and wheat
Hongbo Yan (2009)
Cloning and molecular characterisation of the maize retinoblastoma gene (ZmRBR2)
Manuela Nájera-Martínez (2008)
The role of hexokinase in plant sugar signal transduction and growth and development
W. Xiao (2004)
PAGE: Parametric Analysis of Gene Set Enrichment
Seon-Young Kim (2004)
Soluble Invertase Expression Is an Early Target of Drought Stress during the Critical, Abortion-Sensitive Phase of Young Ovary Development in Maize1
M. Andersen (2002)
Evidence for a role of raffinose in stabilizing photosystem II during freeze–thaw cycles
Markus Knaupp (2011)
ABA-mediated transcriptional regulation in response to osmotic stress in plants
Yasunari Fujita (2011)
Functional Analysis of Maize RAD51 in Meiosis and Double-Strand Break Repair
Jin Li (2007)
The Arabidopsis Abscisic Acid Response Gene ABI5 Encodes a Basic Leucine Zipper Transcription Factor
R. Finkelstein (2000)
Genome-wide analysis of cyclins in maize (Zea mays).
X. Hu (2010)
Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat.
Y. Ruan (2010)
bZIP Research Group (2002) bZIP transcription factors in Arabidopsis
M Jakoby (2002)
Phospholipase D- and phosphatidic acid-mediated signaling in plants.
M. Li (2009)
Three Genes That Affect Sugar Sensing (Abscisic Acid Insensitive 4, Abscisic Acid Insensitive 5, and Constitutive Triple Response 1) Are Differentially Regulated by Glucose in Arabidopsis
A. Becerra (2012)
Characterization of three homologous basic leucine zipper transcription factors (bZIP) of the ABI5 family during Arabidopsis thaliana embryo maturation.
Sandra Bensmihen (2005)
Potato guard cells respond to drying soil by a complex change in the expression of genes related to carbon metabolism and turgor regulation.
J. Kopka (1997)
The Rad17 homologue of Arabidopsis is involved in the regulation of DNA damage repair and homologous recombination.
Fabian Heitzeberg (2004)
Early PLDalpha-mediated events in response to progressive drought stress in Arabidopsis: a transcriptome analysis.
S. Mane (2007)
The cellular language of myo-inositol signaling.
G. Gillaspy (2011)
Starch and the control of kernel number in maize at low water potentials.
C. Zinselmeier (1999)
Cloning and molecular characterisation of the maize retinoblastoma gene ( ZmRBR 2 )
ES Ober (1991)
MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
O. Thimm (2004)
Comparative transcriptional profiling and evolutionary analysis of the GRAM domain family in eukaryotes.
Shu-Ye Jiang (2008)
The ins and outs of the plant cell cycle
L. D. Veylder (2007)
Cytometrical Evidence That the Loss of Seed Weight in theminiature1 Seed Mutant of Maize Is Associated with Reduced Mitotic Activity in the Developing Endosperm1
B. Vilhar (2002)
Positive regulation of minichromosome maintenance gene expression, DNA replication, and cell transformation by a plant retinoblastoma gene
P. Sabelli (2009)
Sugars as Signal Molecules in Plant Seed Development
U. Wobus (1999)
Reactive oxygen species production by potato tuber mitochondria is modulated by mitochondrially bound hexokinase activity
J Camacho-Pereira (2009)
drought stress. The consequence of this is most likely a decrease in Glc levels, one of the products of invertase activity, disrupting the hexose-Suc ratios in the ovary
TopHat: discovering splice junctions with RNA-Seq
C. Trapnell (2009)
Purification and characterization of soluble starch synthases from maize endosperm.
H. Cao (2000)
Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses.
K. Yamaguchi-Shinozaki (2006)
The Barley MLO Modulator of Defense and Cell Death Is Responsive to Biotic and Abiotic Stress Stimuli1
P. Piffanelli (2002)
Identification of novel Mlo family members in wheat and their genetic characterization.
Shogo Konishi (2010)
ROS and redox signalling in the response of plants to abiotic stress.
N. Suzuki (2012)
ADP-glucose pyrophosphorylasedeficient pea embryos reveal specific transcriptional and metabolic changes of carbon-nitrogen metabolism and stress responses
K Weigelt (2009)
The Role of bZIP Transcription Factors in Green Plant Evolution: Adaptive Features Emerging from Four Founder Genes
L. G. Corrêa (2008)
Effects of water-deficit stress on the transcriptomes of developing immature ear and tassel in maize
Yunlong Zhuang (2007)
Comparative studies on the Arabidopsis aldehyde oxidase (AAO) gene family revealed a major role of AAO3 in ABA biosynthesis in seeds.
M. Seo (2004)
RNA-based regulation in the plant circadian clock.
D. Staiger (2011)
Myo-inositol and beyond--emerging networks under stress.
R. Valluru (2011)
tension of the visualization tool MapMan to allow statistical analysis of arrays , display of corresponding genes , and comparison with known responses
B Usadel (2005)
AREB 1 is a transcription activator of novel ABRE - dependent ABA signaling that enhances drought stress tolerance in Arabidopsis
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
K. Livak (2001)
A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication.
G. Grafi (1996)
Specific oxidative cleavage of carotenoids by VP14 of maize.
S. H. Schwartz (1997)
Transcript profiling reveals diverse roles of auxin‐responsive genes during reproductive development and abiotic stress in rice
M. Jain (2009)
Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants.
I. Couée (2006)
bZIP transcription factors in Arabidopsis
J. L. Riechmann (2002)
ABFs, a Family of ABA-responsive Element Binding Factors*
H. Choi (2000)
The contribution of cell cycle regulation to endosperm development
P. Sabelli (2009)
β-Amylase Induction and the Protective Role of Maltose during Temperature Shock1
F. Kaplan (2004)
Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine.
Y. Li (2006)
Sugar signalling and antioxidant network connections in plant cells
Mohammad Reza Bolouri-Moghaddam (2010)
Comparative Transcriptional Profiling of Placenta and Endosperm in Developing Maize Kernels in Response to Water Deficit1
Long-Xi Yu (2003)
PIP 5 K 9 , an Arabidopsis phosphatidylinositol monophosphate kinase , interacts with a cytosolic invertase to negatively regulate sugar - mediated root growth
SP Mane (2008)
PIP5K9, an Arabidopsis Phosphatidylinositol Monophosphate Kinase, Interacts with a Cytosolic Invertase to Negatively Regulate Sugar-Mediated Root Growth[W]
Y. Lou (2007)
Cyclin-dependent kinase inhibitors in maize endosperm and their potential role in endoreduplication
CM Coelho (2005)
Genetic association mapping identifies single nucleotide polymorphisms in genes that affect abscisic acid levels in maize floral tissues during drought
T. Setter (2011)
Abscisic Acid Signaling in Seeds and Seedlings Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010441.
R. Finkelstein (2002)
Arabidopsis Basic Leucine Zipper Proteins That Mediate Stress-Responsive Abscisic Acid Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010362.
J. Kang (2002)
40 " " microarray analysis and promoter classification using a Relevance Vector Machine
KJ Livak (2001)
b-Amylase induction and the protective role of maltose during temperature shock
F Kaplan (2004)
Genetic control of cell wall invertases in developing endosperm of maize
P. Chourey (2005)
Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm.
T. Setter (2001)
Characterization of SSIIIa-Deficient Mutants of Rice: The Function of SSIIIa and Pleiotropic Effects by SSIIIa Deficiency in the Rice Endosperm[C][OA]
N. Fujita (2007)
An Invertase Inhibitor from Maize Localizes to the Embryo Surrounding Region during Early Kernel Development
N. Bate (2004)
beta - Amylase induction and the protective role of maltose during temperature shock
F Kaplan (2004)
Isolation and analysis of water stress induced genes in maize seedlings by subtractive PCR and cDNA macroarray
J. Zheng (2004)
AREB1 Is a Transcription Activator of Novel ABRE-Dependent ABA Signaling That Enhances Drought Stress Tolerance in Arabidopsis[W][OA]
Yasunari Fujita (2005)
potato. Several genes known to be involved in Suc processing were differentially expressed under drought, confirming earlier observations
The Maize Homologue of the Cell Cycle Checkpoint Protein MAD2 Reveals Kinetochore Substructure and Contrasting Mitotic and Meiotic Localization Patterns
H. Yu (1999)
Neutral invertase, hexokinase and mitochondrial ROS homeostasis
L. Xiang (2011)
Metabolic sugar signal promotes Arabidopsis meristematic proliferation via G2.
A. Skylar (2011)
Cyclin dependent protein kinases and stress responses in plants
Georgios Kitsios (2011)
Influence of water deficit on maize endosperm development : enzyme activities and RNA transcripts of starch and zein synthesis, abscisic Acid, and cell division.
E. Ober (1991)
Extension of the Visualization Tool MapMan to Allow Statistical Analysis of Arrays, Display of Coresponding Genes, and Comparison with Known Responses1
B. Usadel (2005)
Engineering seed dormancy by the modification of zeaxanthin epoxidase gene expression
A. Frey (2004)
Molecular and physiological adaptation to prolonged drought stress in the leaves of two Andean potato genotypes.
S. Mane (2008)
who observed a lower level of starch in water-stressed ovaries. In cereals, GBSSI is encoded by the Waxy (Wx) locus, and the role of GBSSI is mostly confined to storage tissues
Abiotic stress and control of grain number in cereals.
R. Dolferus (2011)
ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice.
S. Oliver (2007)
Low Glucose Uncouples Hexokinase1-Dependent Sugar Signaling from Stress and Defense Hormone Abscisic Acid and C2H4 Responses in Arabidopsis1[C][W]
Young-Hee Cho (2009)
This paper is referenced by
“Omics” of Maize Stress Response for Sustainable Food Production: Opportunities and Challenges
The Lesion Simulating Disease (LSD) gene family as a variable in soybean response to Phakopsora pachyrhizi infection and dehydration
Caroline Cabreira (2013)
Effects of drought and salt-stresses on gene expression in Caragana korshinskii seedlings revealed by RNA-seq
Shaofeng Li (2016)
Molecular Analysis of Oil Palm (Elaeis guineensis Jacq.) Flowering Associated Genes and their Potential Application in Breeding Programmes
Walter Ajambang Nchu (2015)
Exploiting Historical Data and Diverse Germplasm to Increase Maize Grain Yield in Texas
Barrero Farfan (2013)
Catalyzing plant science research with RNA-seq
Laetitia B B Martin (2013)
De Novo Transcriptome Assembly and Comparative Analysis of Differentially Expressed Genes in Prunus dulcis Mill. in Response to Freezing Stress
S. Mousavi (2014)
Drought responsive genes and their functional terms identified by GS FLX Pyro sequencing in maize.
Utlwang Batlang (2014)
Identification of candidate genes for drought tolerance by whole-genome resequencing in maize
J. Xu (2013)
Sterility Caused by Floral Organ Degeneration and Abiotic Stresses in Arabidopsis and Cereal Grains
Ashley R. Smith (2016)
Abiotic Stress Biology in Horticultural Plants
Y. Kanayama (2015)
Gene expression profiling of Bothriochloa ischaemum leaves and roots under drought stress.
Chunyan Li (2019)
RNA-Seq Based Analysis of Population Structure within the Maize Inbred B73
Zhikai Liang (2016)
Effects of maize organ-specific drought stress response on yields from transcriptome analysis
Baomei Wang (2019)
Characterization of genes involved in lignin biosynthesis in Tectona grandis
Esteban Galeano Gómez (2015)
Comparative Gene Expression Analysis of Seed Development in Waxy and Dent Corn (Zea mays L.)
K. J. Sa (2018)
Selection of reference genes for flowering pathway analysis in the masting plants, Celmisia lyallii and Chionochloa pallens, under variable environmental conditions
RNA-Seq Data Analysis for Studying Abiotic Stress in Horticultural Plants
V. Mironova (2015)
Science behind biostimulant action of seaweed extract on growth and crop yield: insights into transcriptional changes in roots of maize treated with Kappaphycus alvarezii seaweed extract under soil moisture stressed conditions
Ranjeet Kumar (2019)
Prediction and characterization of transcription factors involved in drought stress response
Chirag Gupta (2020)
Transcriptome characterization and differential expression analysis of cold-responsive genes in young spikes of common wheat.
Shujuan Zhang (2014)
YeATS - a tool suite for analyzing RNA-seq derived transcriptome identifies a highly transcribed putative extensin in heartwood/sapwood transition zone in black walnut.
S. Chakraborty (2015)
A higher sink competitiveness of the rooting zone and invertases are involved in dark stimulation of adventitious root formation in Petunia hybrida cuttings.
Y. Klopotek (2016)
Improving Maize Production under Drought Stress Traits, Screening Methods, and Environments
Gerald De La Fuente (2014)
Functional mechanisms of drought tolerance in subtropical maize (Zea mays L.) identified using genome-wide association mapping
Nepolean Thirunavukkarasu (2014)
Large-scale transcriptional profiling of lignified tissues in Tectona grandis
Esteban Galeano (2015)
Dehydration induced transcriptomic responses in two Tibetan hulless barley (Hordeum vulgare var. nudum) accessions distinguished by drought tolerance
Junjun Liang (2017)
Identification, Characterization, and Functional Validation of Drought-responsive MicroRNAs in Subtropical Maize Inbreds
J. Aravind (2017)
Genome-wide identification of gene expression in contrasting maize inbred lines under field drought conditions reveals the significance of transcription factors in drought tolerance
X. Zhang (2017)
YeATS - a tool suite for analyzing RNA-seq derived transcriptome identifies a highly transcribed putative extensin in heartwood/sapwood transition zone in black walnut
S. Chakraborty (2015)
The Agony of Choice: How Plants Balance Growth and Survival under Water-Limiting Conditions1
H. Claeys (2013)
Functional Genomics of Biotic and Abiotic Stresses in Phaseolus vulgaris
D. G. G. Caldas (2016)See more