The developmental dynamics of the maize leaf transcriptome

We have analyzed the maize leaf transcriptome using Illumina sequencing. We mapped more than 120 million reads to define gene structure and alternative splicing events and to quantify transcript abundance along a leaf developmental gradient and in mature bundle sheath and mesophyll cells. We detected differential mRNA processing events for most maize genes. We found that 64% and 21% of genes were differentially expressed along the developmental gradient and between bundle sheath and mesophyll cells, respectively. We implemented Gbrowse, an electronic fluorescent pictograph browser, and created a two-cell biochemical pathway viewer to visualize datasets. Cluster analysis of the data revealed a dynamic transcriptome, with transcripts for primary cell wall and basic cellular metabolism at the leaf base transitioning to transcripts for secondary cell wall biosynthesis and C4 photosynthetic development toward the tip. This dataset will serve as the foundation for a systems biology approach to the understanding of photosynthetic development.

[1]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[2]  W. Majeran,et al.  Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomicsw⃞ , 2005, The Plant Cell Online.

[3]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[4]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[5]  Richard W. Twigg,et al.  Specification of adaxial cell fate during maize leaf development , 2004, Development.

[6]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[7]  Michelle T. Juarez,et al.  microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity , 2004, Nature.

[8]  J. Langdale,et al.  GOLDEN 2: A Novel Transcriptional Regulator of Cellular Differentiation in the Maize Leaf , 1998, Plant Cell.

[9]  W. Majeran,et al.  Reconstruction of Metabolic Pathways, Protein Expression, and Homeostasis Machineries across Maize Bundle Sheath and Mesophyll Chloroplasts: Large-Scale Quantitative Proteomics Using the First Maize Genome Assembly1[W][OA] , 2010, Plant Physiology.

[10]  T. Brutnell,et al.  A multi-treatment experimental system to examine photosynthetic differentiation in the maize leaf , 2007, BMC Genomics.

[11]  M. D. Hatch,et al.  Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. , 1966, The Biochemical journal.

[12]  Daeyoup Lee,et al.  Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. , 2009, The Plant journal : for cell and molecular biology.

[13]  W. W. Bailey The Grasses , 1871, The American Naturalist.

[14]  Dominique C. Bergmann,et al.  Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses , 2009, Development.

[15]  B. Williams,et al.  Mapping and quantifying mammalian transcriptomes by RNA-Seq , 2008, Nature Methods.

[16]  T. Helentjaris,et al.  TRM1, a YY1-like suppressor of rbcS-m3 expression in maize mesophyll cells , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Dan Nettleton,et al.  Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.) , 2007, The Plant journal : for cell and molecular biology.

[18]  S. Yanagisawa,et al.  Involvement of Maize Dof Zinc Finger Proteins in Tissue-Specific and Light-Regulated Gene Expression , 1998, Plant Cell.

[19]  H. Bohnert,et al.  Arabidopsis transcript and metabolite profiles: ecotype-specific responses to open-air elevated [CO2]. , 2008, Plant, cell & environment.

[20]  J. Ohlrogge,et al.  Identification of an Arabidopsis Feruloyl-Coenzyme A Transferase Required for Suberin Synthesis1[W][OA] , 2009, Plant Physiology.

[21]  R. Poethig,et al.  Clonal analysis of leaf development in maize , 1995 .

[22]  Volker Brendel,et al.  Cross-species EST alignments reveal novel and conserved alternative splicing events in legumes , 2008, BMC Plant Biology.

[23]  J. Sheen C4 GENE EXPRESSION. , 2003, Annual review of plant physiology and plant molecular biology.

[24]  W. Barbazuk,et al.  Genome-wide analyses of alternative splicing in plants: opportunities and challenges. , 2008, Genome research.

[25]  M. Rumsby,et al.  Plastid differentiation, acyl lipid, and Fatty Acid changes in developing green maize leaves. , 1973, Plant physiology.

[26]  B. C. Sharman,et al.  Developmental Anatomy of the Shoot of Zea mays L , 1942 .

[27]  Grantley W Lycett The role of Rab GTPases in cell wall metabolism. , 2008, Journal of experimental botany.

[28]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[29]  M. Freeling,et al.  Division and differentiation during normal and liguleless-1 maize leaf development. , 1990, Development.

[30]  Henry D. Priest,et al.  Genome-wide mapping of alternative splicing in Arabidopsis thaliana. , 2010, Genome research.

[31]  J. Chory,et al.  Coordination of gene expression between organellar and nuclear genomes , 2008, Nature Reviews Genetics.

[32]  K. Esau Ontogeny of the vascular bundle in Zea Mays , 1943 .

[33]  M. Tsiantis,et al.  A KNOX family TALE. , 2009, Current opinion in plant biology.

[34]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[35]  S. Long,et al.  What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? , 2008, Current opinion in biotechnology.

[36]  Ann Allergy,et al.  O R I G I N a L a R T I C L E S , 2022 .

[37]  W. Majeran,et al.  Consequences of C4 Differentiation for Chloroplast Membrane Proteomes in Maize Mesophyll and Bundle Sheath Cells *S , 2008, Molecular & Cellular Proteomics.

[38]  A. Bosabalidis,et al.  Anatomical and Ultrastructural Changes Associated with Sink-to-Source Transition in Developing Maize Leaves , 1996, International Journal of Plant Sciences.

[39]  R. Turgeon,et al.  Phloem Loading Strategies in Three Plant Species That Transport Sugar Alcohols1[C][OA] , 2009, Plant Physiology.

[40]  J. Hibberd The evolution of C4 photosynthesis , 2009 .

[41]  S. Kirchanski THE ULTRASTRUCTURAL DEVELOPMENT OF THE DIMORPHIC PLASTIDS OF ZEA MAYS L. , 1975 .

[42]  S. Lewis,et al.  The generic genome browser: a building block for a model organism system database. , 2002, Genome research.

[43]  Michael Snyder,et al.  Systems biology from a yeast omics perspective , 2009, FEBS letters.

[44]  Daniel L. Mace,et al.  A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns , 2007, Science.

[45]  Przemyslaw Prusinkiewicz,et al.  Integration of transport-based models for phyllotaxis and midvein formation. , 2009, Genes & development.

[46]  D. Chitwood,et al.  Signals and prepatterns: new insights into organ polarity in plants. , 2009, Genes & development.

[47]  Chen,et al.  Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize , 1999, Plant physiology.

[48]  Xiaohong Yu,et al.  A hydroxycinnamoyltransferase responsible for synthesizing suberin aromatics in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[49]  V. Brendel,et al.  Genomewide comparative analysis of alternative splicing in plants. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  M. Stephens,et al.  RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. , 2008, Genome research.

[51]  M. Hedger,et al.  Effects of chronic celecoxib on testicular function in normal and lipopolysaccharide-treated rats. , 2009, International journal of andrology.

[52]  E. López-Juez,et al.  Plastids unleashed: their development and their integration in plant development. , 2005, The International journal of developmental biology.

[53]  B. Usadel,et al.  Xeml Lab: a tool that supports the design of experiments at a graphical interface and generates computer-readable metadata files, which capture information about genotypes, growth conditions, environmental perturbations and sampling strategy. , 2009, Plant, cell & environment.

[54]  W. Stiekema,et al.  Comparative analysis indicates that alternative splicing in plants has a limited role in functional expansion of the proteome , 2009, BMC Genomics.