Plant Molecular Biology

, Volume 60, Issue 3, pp 343–363 | Cite as

Transcription Profile Analyses Identify Genes and Pathways Central to Root Cap Functions in Maize

  • Keni Jiang
  • Shibo Zhang
  • Stanley Lee
  • George Tsai
  • Kyungpil Kim
  • Haiyan Huang
  • Charles Chilcott
  • Tong Zhu
  • Lewis J. Feldman
Article

Abstract

Affymetrix GeneChips arrayed with about one-half (~23K) of the rice genes were used to profile gene transcription activity in three tissues comprising the maize root tip; the proximal meristem (PM), the quiescent center (QC), and the root cap (RC). Here we analyze the gene transcription profile of the RC, compared to both the PM and the QC, from three biological replicates. In the RC, a total of 669 genes were identified as being differentially upregulated, and 365 differentially downregulated. Real-time quantitative RT-PCR analysis was used to confirm upregulated genes in the RC. In addition, using the technique of laser microdissection (LMD) we localized upregulated gene expression to the lateral RC cells. Taken as a whole, transcription profile analyses revealed the upregulation in the maize RC of clusters of genes linked to major metabolic processes and pathways, including: (1) transport, both the export of carbohydrates and the uptake of nutrients; (2) sensing and responding to (often stressful) biotic and abiotic environmental stimuli; (3) integrating the responses of at least 3 major growth regulators (auxin, ethylene, jasmonic acid); (4) processing the large amount of carbohydrate transported into the RC. Although the profile data are derived using heterologous rice GeneChips, with about half of the total rice gene set, this study, nevertheless, provides a genomic scale characterization of the entire RC, and serves as a new platform from which to advance studies of the network of pathways operating in the maize RC.

Key words

maize microarray root cap transcription profile 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

supp1.xls (354 kb)
Supplementary material
supp2.xls (196 kb)
Supplementary material
supp3.doc (112 kb)
Supplementary material

References

  1. Abel, S., Nguyen, M.D., Theologis, A. 1995The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thalianaJ. Mol. Biol.251533549CrossRefPubMedGoogle Scholar
  2. Agaphonov, M.O., Packeiser, A.N., Chechenova, M.B., Choi, E.S., Ter-Avanesyan, M.D. 2001Mutation of the homologue of GDP-mannose pyrophosphorylase alters cell wall structure, protein glycosylation and secretion in Hansenula polymorphaYeast18391402CrossRefPubMedGoogle Scholar
  3. Arango, M., Gevaudant, F., Oufattole, M., Boutry, M. 2003The plasma membrane proton pump ATPase: the significance of gene subfamiliesPlanta216355365PubMedGoogle Scholar
  4. Bacic, A., Moody, S.F., Clarke, A.E. 1986Structural analysis of secreted root slime from maize (Zea mays L.)Plant Physiol.80771777Google Scholar
  5. Baluska, F., Volkmann, D., Hauskrecht, M., Barlow, P.W. 1996Root cap mucilage and extracellular calcium as modulators of cellular growth in postmitotic growth zones of the maize root apexBot. Acta.1092534Google Scholar
  6. Bennetzen, J.L., Coleman, C., Liu, R., Ma, J., Ramakrishna, W. 2004Consistent over-estimation of gene number in complex plant genomesCurr. Opin. Plant Biol.7732736CrossRefPubMedGoogle Scholar
  7. Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung, J.W., Lambert, G.M., Galbraith, D.W., Benfey, P.N. 2003A gene expression map of the Arabidopsis rootScience30219561960CrossRefPubMedGoogle Scholar
  8. Bonin, C.P., Potter, I., Vanzin, G.F., Reiter, W.D. 1997The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucoseProc Natl. Acad. Sci. USA9420852090CrossRefPubMedGoogle Scholar
  9. Bonin, C.P., Reiter, W.D. 2000A bifunctional epimerase-reductase acts downstream of the MUR1 gene product and completes the de novo synthesis of GDP-L-fucose in ArabidopsisPlant J.21445454CrossRefPubMedGoogle Scholar
  10. Brigham, L.A., Woo, H.H., Nicoll, S.M., Hawes, M.C. 1995Differential expression of proteins and mRNAs from border cells and root tips of peaPlant Physiol.109457463PubMedGoogle Scholar
  11. Carroll, A.D., Moyen, C., Kesteren, P.V., Tooke, F., Battey, N.H., Brownelee, C. 1998Ca2+, annexins, and GTP modulate exocytosis from maize root cap protoplastsPlant Cell1012671276CrossRefPubMedGoogle Scholar
  12. Chaboud, A. 1983Isolation, purification and chemical composition of maize root cap slimePlant Soil73395402CrossRefGoogle Scholar
  13. Chaboud, A., Rougier, M. 1984Identification and localization of sugar components of rice (Oryza sativa L.) root cap mucilageJ. Plant Physiol.116323330Google Scholar
  14. Che, P., Gingerich, D.J., Lall, S., Howell, S.H. 2002Global and hormone-induced gene expression changes during shoot development in ArabidopsisPlant Cell1427712785CrossRefPubMedGoogle Scholar
  15. Chen, J.G., Ullah, H., Young, J.C., Sussman, M.R., Jones, A.M. 2001ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesisGenes Dev.15902911PubMedGoogle Scholar
  16. Chinchilla, D., Merchan, F., Megias, M., Kondorosi, A., Sousa, C., Crespi, M. 2003Ankyrin protein kinases: a novel type of plant kinase gene whose expression is induced by osmotic stress in alfalfaPlant Mol. Biol.51555566CrossRefPubMedGoogle Scholar
  17. Eapen, D., Barroso, M.L., Campos, M.E., Ponce, G., Corkidi, G., Dubrovsky, J.G., Cassab, G.I. 2003A no hydrotropic response root mutant that responds positively to gravitropism in ArabidopsisPlant Physiol.131536546CrossRefPubMedGoogle Scholar
  18. Endege, W.O., Steinmann, K.E., Boardman, L.A., Thibodeau, S.N., Schlegel, R. 1999Representative cDNA libraries and their utility in gene expression profilingBiotechniques26542550PubMedGoogle Scholar
  19. Friml, J., Wisniewska, J., Benková, E, Mendgen, K., Palme, K. 2002Lateral relocation of auxin efflux regulator PIN3 mediates tropism in ArabidopsisNature415806809PubMedGoogle Scholar
  20. Goff, S.A., Ricke, D., Lan, T-H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., Hadley, D., Hutchison, D., Martin, C., Katagiri, F., Lange, B.M., Moughamer, T., Xia, Y., Budworth, P., Zhong, J., Miguel, T., Paszkowski, U., Zhang, S., Colbert, M., Sun, W-L., Chen, L., Cooper, B., Park, S., Wood, T.C., Mao, L., Quail, P., Wing, R., Dean, R., Yu, Y., Zharkikh, A., Shen, R., Sahasrabudhe, S., Thomas, A., Cannings, R., Gutin, A., Pruss, D., Reid, J., Tavtigian, S., Mitchell, J., Eldredge, G., Scholl, T., Miller, R., Bhatnagar, S., Adey, N., Rubano, T., Tusneem, N., Robinson, R., Feldhaus, J., Macalma, T., Oliphant, A., Briggs, S. 2002A draft sequence of the rice genome (Oryza sativa L. ssp. japonica)Science29692100CrossRefPubMedGoogle Scholar
  21. Grossman, K., Rosenthal, C., Kwiatkowski, J. 2004Increases in jasmonic acid caused by indole-3-acetic acid and auxin herbicides in cleavers (Galium aparine)J. Plant Physiol.161809814Google Scholar
  22. Guinel, F.C., McCully, M.E. 1987The cells shed by the root cap of Zea: their origin and some structural and physiological propertiesPlant Cell Environ.10565578Google Scholar
  23. Guo, H., Ecker, J.R. 2004The ethylene signaling pathway: New insightsCurr. Opin. Plant Biol.74049CrossRefPubMedGoogle Scholar
  24. Hamann, T., Mayer, U., Jürgens, G. 1999The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryoDevelopment12613871395PubMedGoogle Scholar
  25. Hamann, T., Benkova, E., Bäurle, I., Kientz, M., Jürgens, G. 2002The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterningGenes Dev.1616101615CrossRefPubMedGoogle Scholar
  26. Haran, S., Logendra, S., Seskar, M., Bratanova, M., Raskin, I. 2000Characterization of Arabidopsis acid phosphatase promoter and regulation of acid phosphatase expressionPlant Physiol.124615626CrossRefPubMedGoogle Scholar
  27. Hawes, M.C., Wheeler, H.E. 1982Factors affecting victorin-induced cell death: temperature and plasmolysisPhysiol. Plant Pathol.20137144Google Scholar
  28. Hawes, M.C., Pueppke, S.G. 1986Sloughed peripheral root cap cells: yield from different species and callus formation from single cellsAm. J. Bot.7314661473Google Scholar
  29. Hawes, M.C., Brigham, L.A., Wen, F., Woo, H., Zhu, Y. 1998Function of root border cells in plant health: pioneers in the rhizosphereAnnu. Rev. Phytopathol.36311327CrossRefPubMedGoogle Scholar
  30. Hawes, M.C., Bengough, G., Cassab, G., Ponce, G. 2003Root caps and rhizosphereJ. Plant Growth Regul.21352367CrossRefGoogle Scholar
  31. Jiang, K., Feldman, L.J. 2003aRoot meristem establishment and maintenance: the role of auxinJ. Plant Growth Regul.21432440CrossRefGoogle Scholar
  32. Jiang, K., Meng, Y.L., Feldman, L.J. 2003bQuiescent center formation is associated with an auxin-regulated oxidizing environmentDevelopment13014291438Google Scholar
  33. Jolliffe, I.T. 1986Principal Component AnalysisSpringerNew YorkGoogle Scholar
  34. Jonak, C., Okresz, L., Bogre, L., Hirt, H. 2002Complexity, cross talk and integration of plant MAP kinase signalingCurr. Opin. Plant Biol.5415424CrossRefPubMedGoogle Scholar
  35. Koch, K. 2004Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant developmentCurr. Opin. Plant Biol.7235246CrossRefPubMedGoogle Scholar
  36. Le Roch, K.G., Zhou, Y.Y., Blair, P.L., Grainger, M., Moch, J.K., Haynes, J.D., la Vega, P., Holder, A.A., Batalov, S., Carucci, D.J., Winzeler, E.A. 2003Discovery of gene function by expression profiling of the malaria parasite life cycleScience30115031508CrossRefPubMedGoogle Scholar
  37. Lee, Y., Choi, D., Kende, H. 2001Expansins: ever-expanding numbers and functionsCurr. Opin. Plant Biol.4527532CrossRefPubMedGoogle Scholar
  38. Lukowitz, W., Nickle, T.C., Meinke, D.W., Last, R.L., Conklin, P.L., Somerville, C.R. 2001Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesisProc. Natl. Acad. Sci. USA9822622267CrossRefPubMedGoogle Scholar
  39. Matsuyama, T., Yasumura, N., Funakoshi, M., Yamada, Y., Hashimoto, T. 1999aMaize genes specifically expressed in the outermost cells of root capPlant Cell Physiol.40469476Google Scholar
  40. Matsuyama, T., Satoh, H., Yamada, Y., Hashimoto, T. 1999bA maize glycine-rich protein is synthesized in the lateral root cap and accumulates in the mucilagePlant Physiol.120665674CrossRefGoogle Scholar
  41. Miller, S.S., Liu, J., Allan, D.L., Menzhuber, C.J., Fedorova, M., Vance, C.P. 2001Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupinPlant Physiol.127594606CrossRefPubMedGoogle Scholar
  42. Nickle, T.C., Meinke, D.W. 1998A cytokinesis-defective mutant of Arabidopsis (cyt1) characterized by embryonic lethality, incomplete cell walls and excessive callose accumulationPlant J.15321332CrossRefPubMedGoogle Scholar
  43. Orozco-Cárdenas, M.L., Narváez-Vásquez, J., Ryan, C.A. 2001Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonatePlant Cell13179191PubMedGoogle Scholar
  44. Ponce, G., Lujan, R., Campos, M.E., Reyes, A., Nieto-Sotelo, J., Feldman, L.J., Cassab, G.I. 2000Three maize root-specific genes are not correctly expressed in regenerated caps in the absence of the quiescent centerPlanta2112333PubMedGoogle Scholar
  45. Rao, M.V., Lee, H.I., Davis, K.R. 2002Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell deathPlant J.32447456CrossRefPubMedGoogle Scholar
  46. Roitsch, T. 1999Source-sink regulation by sugar and stressCurr. Opin. Plant Biol.2198206CrossRefPubMedGoogle Scholar
  47. Roitsch, T., Gonzalez, M-C. 2004Function and regulation of plant invertases: sweet sensationsTrends Plant Sci.9606613CrossRefPubMedGoogle Scholar
  48. Rolland, F., Sheen, J. 2005Sugar sensing and signalling networks in plantsBiochem. Soc. Trans.33269271PubMedGoogle Scholar
  49. Russell, S. 1977Plant Root SystemsMcGraw-Hill Book Company (UK) LimitedLondon, UKGoogle Scholar
  50. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P., Scheres, B. 1999An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis rootCell99463472CrossRefPubMedGoogle Scholar
  51. Schopfer, P., Liszkay, A., Bechtold, M., Frahry, G., Wagner, A. 2002Evidence that hydroxyl radicals mediate auxin-induced extension growthPlanta214821828CrossRefPubMedGoogle Scholar
  52. Simpson, K.M., Baum, J., Good, R.T., Winzeler, E.A., Cowman, A.F., Speed, T.P. 2005A comparison of match-only algorithms for the analysis of Plasmodium falciparum oligonucleotide arraysIntern. J. Parasitol.35523531Google Scholar
  53. Stephenson, M.B., Hawes, M.C. 1994Correlation of pectin methylesterase activity in root caps of pea with root border cell separationPlant Physiol.106739745PubMedGoogle Scholar
  54. Swarup, R., Friml, J., Marchant, A., Ljung, K., Sandberg, G., Palme, K., Bennett, M. 2001Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apexGenes Dev.1526482653CrossRefPubMedGoogle Scholar
  55. Tetlow, I.J., Morell, M.K., Emes, M.J. 2004Recent developments in understanding the regulation of starch metabolism in higher plantsJ. Exp. Bot.5521312145CrossRefPubMedGoogle Scholar
  56. Tiwari, S.B., Wang, X.J., Hagen, G., Guilfoyle, T.J. 2001AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxinPlant Cell1328092822CrossRefPubMedGoogle Scholar
  57. Tsuchisaka, A., Theologis, A. 2004Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family membersPlant Physiol.13629823000CrossRefPubMedGoogle Scholar
  58. Tsugeki, R., Fedoroff, N.V. 1999Genetic ablation of root cap cells in ArabidopsisProc. Natl. Acad. Sci. USA961294112946CrossRefPubMedGoogle Scholar
  59. Turner, J.G., Ellis, C., Devoto, A. 2002The jasmonate signal pathwayPlant CellSuppliment S153S164Google Scholar
  60. Wang, H., Li, J., Bostock, R.M., Gilchrist, D.G. 1996Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during developmentPlant Cell8375391PubMedGoogle Scholar
  61. Wen, F., Zhu, Y., Hawes, M.C. 1999Effect of pectin methylesterase gene expression on pea root developmentPlant Cell1111291140PubMedGoogle Scholar
  62. Wong, J.H., Balmer, Y., Cai, N., Tanaka, C.K., Vensel, W.H., Hurkman, W.J., Buchanan, B.B. 2003Unraveling thioredoxin-linked metabolic processes of cereal starchy endosperm using proteomicsFEBS Lett.547151156CrossRefPubMedGoogle Scholar
  63. Woo, H.H., Orbach, M.J., Hirsch, A.M., Hawes, M.C. 1999Meristem-localized inducible expression of a UDP-glycosyltransferase gene is essential for growth and development in pea and alfalfaPlant Cell1123032315CrossRefPubMedGoogle Scholar
  64. Wright, K., Northcote, D.H. 1974The relationship of root-cap slimes to pectinsBiochemical J.139525534Google Scholar
  65. Yamagami, T., Tsuchisaka, A., Yamada, K., Haddon, W.F., Harden, L.A., Theologis, A. 2003Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene familyJ. Biol. Chem.2784910249112CrossRefPubMedGoogle Scholar
  66. Yang, H.J., Shen, H., Chen, L., Xing, Y.Y., Wang, Z.Y., Zhang, J.L., Hong, M.M. 2002The OsEBP-89 gene of rice encodes a putative EREBP transcription factor and is temporally expressed in developing endosperm and intercalary meristemPlant Mol. Biol.50379391CrossRefPubMedGoogle Scholar
  67. Yang, S., Hoffman, N. 1984Ethylene biosynthesis and its regulation in higher plantsAnnu. Rev. Plant Physiol.35155189CrossRefGoogle Scholar
  68. Yan, J., Wang, J., Zhang, H. 2002An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolismPlant J.29193202CrossRefPubMedGoogle Scholar
  69. Yuen, C.Y.L., Sedbrook, J.C., Perrin, R.M., Carroll, K.L., Masson, P.KH. 2005Loss-of-function mutations of ROOT HAIR DEFECTIVE3 suppress root waving, skewing, and epidermal cell file rotation in ArabidopsisPlant Physiol.138701714CrossRefPubMedGoogle Scholar
  70. Zhang, W.C., Yan, W.M. 1995Detachment of root cap cells of maize and its effects on relationship between root and rhizosphereActa. Phytophysiol. Sin.21340346Google Scholar
  71. Zhou, Y., Abagyan, R. 2002Match-only integral distribution (MOID) algorithm for high-density oligonucleotide array analysisBMC Bioinformatics3115CrossRefGoogle Scholar
  72. Zhu, T., Rost, T.L. 2000Directional cell-to-cell communication in the Arabidopsis root apical meristem. III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks after germinationProtoplasma21399107CrossRefGoogle Scholar
  73. Zhu, T., Chang, H.-S., Schmeits, J., Gil, P., Shi, L., Budworth, P., Zou, G., Chen, X., Wang, X. 2001Gene expression microarrays: Improvements and applications towards agricultural gene discoveryJ. Assoc. Lab. Automat.69598Google Scholar
  74. Zhu, T., Budworth, P., Chen, W., Provart, N., Chang, H.-S., Guimil, S., Su, W.P., Zou, G., Wang, X. 2003Transcriptional control of nutrient partitioning during rice grain fillingPlant Biotechnol. J.15970Google Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Keni Jiang
    • 1
  • Shibo Zhang
    • 1
  • Stanley Lee
    • 1
  • George Tsai
    • 1
  • Kyungpil Kim
    • 2
  • Haiyan Huang
    • 2
  • Charles Chilcott
    • 3
  • Tong Zhu
    • 3
  • Lewis J. Feldman
    • 1
  1. 1.Department of Plant and Microbial BiologyUniversity of CaliforniaBerkeleyUSA
  2. 2.Department of StatisticsUniversity of CaliforniaBerkeleyUSA
  3. 3.Syngenta Biotechnology, Inc.Research Triangle ParkUSA

Personalised recommendations