Developmental Dynamics of Kranz Cell Transcriptional Specificity in Maize Leaf Reveals Early Onset of C4-related Processes

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2014 May 3

PMID 24790109

Citations 41

Authors

S Lori Tausta

Pinghua Li

Yaqing Si

Neeru Gandotra

Peng Liu

Qi Sun

Thomas P Brutnell

Timothy Nelson

Affiliations

Soon will be listed here.

Abstract

The comparison of the cell-specific transcriptomes of bundle sheath (BS) and mesophyll (M) cells from successive developmental stages of maize (Zea mays) leaves reveals that the number of genes preferentially transcribed in one cell type or the other varies considerably from the sink-source transition to mature photosynthetic stages. The number of differentially expressed (DE) genes is maximal at a stage well before full maturity, including those that encode key functions for C4 photosynthesis. The developmental dynamics of BS/M differential expression can be used to identify candidates for other C4-related functions and to simplify the identification of specific pathways members from otherwise complex gene families. A significant portion of the candidates for C4-related transcription factors identified with this developmental DE strategy overlap with those identified in studies using alternative strategies, thus providing independent support for their potential importance.

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References

Hanba Y, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I . Overexpression of the barley aquaporin HvPIP2;1 increases internal CO(2) conductance and CO(2) assimilation in the leaves of transgenic rice plants. Plant Cell Physiol. 2004; 45(5):521-9. DOI: 10.1093/pcp/pch070. View

Takabayashi A, Kishine M, Asada K, Endo T, Sato F . Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis. Proc Natl Acad Sci U S A. 2005; 102(46):16898-903. PMC: 1283823. DOI: 10.1073/pnas.0507095102. View

HALL L, Roth R, Brutnell T, Langdale J . Cellular differentiation in the maize leaf is disrupted by bundle sheath defective mutations. Symp Soc Exp Biol. 2000; 51:27-31. View

Friso G, Majeran W, Huang M, Sun Q, van Wijk K . 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 assembly. Plant Physiol. 2010; 152(3):1219-50. PMC: 2832236. DOI: 10.1104/pp.109.152694. View

Su Y, Frommer W, Ludewig U . Molecular and functional characterization of a family of amino acid transporters from Arabidopsis. Plant Physiol. 2004; 136(2):3104-13. PMC: 523371. DOI: 10.1104/pp.104.045278. View

Wang H, Dixon R . On-off switches for secondary cell wall biosynthesis. Mol Plant. 2011; 5(2):297-303. DOI: 10.1093/mp/ssr098. View

Johansson I, Karlsson M, Johanson U, Larsson C, Kjellbom P . The role of aquaporins in cellular and whole plant water balance. Biochim Biophys Acta. 2000; 1465(1-2):324-42. DOI: 10.1016/s0005-2736(00)00147-4. View

Bowman S, Patel M, Yerramsetty P, Mure C, Zielinski A, Bruenn J . A novel RNA binding protein affects rbcL gene expression and is specific to bundle sheath chloroplasts in C4 plants. BMC Plant Biol. 2013; 13:138. PMC: 3849040. DOI: 10.1186/1471-2229-13-138. View

Maekawa S, Sato T, Asada Y, Yasuda S, Yoshida M, Chiba Y . The Arabidopsis ubiquitin ligases ATL31 and ATL6 control the defense response as well as the carbon/nitrogen response. Plant Mol Biol. 2012; 79(3):217-27. DOI: 10.1007/s11103-012-9907-0. View

10.

Jiang Y, Yang B, Deyholos M . Functional characterization of the Arabidopsis bHLH92 transcription factor in abiotic stress. Mol Genet Genomics. 2009; 282(5):503-16. DOI: 10.1007/s00438-009-0481-3. View

11.

Gandotra N, Coughlan S, Nelson T . The Arabidopsis leaf provascular cell transcriptome is enriched in genes with roles in vein patterning. Plant J. 2013; 74(1):48-58. DOI: 10.1111/tpj.12100. View

12.

Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K . NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell. 2007; 19(1):270-80. PMC: 1820955. DOI: 10.1105/tpc.106.047043. View

13.

Fragoso S, Espindola L, Paez-Valencia J, Gamboa A, Camacho Y, Martinez-Barajas E . SnRK1 isoforms AKIN10 and AKIN11 are differentially regulated in Arabidopsis plants under phosphate starvation. Plant Physiol. 2009; 149(4):1906-16. PMC: 2663738. DOI: 10.1104/pp.108.133298. View

14.

Tomcal M, Stiffler N, Barkan A . POGs2: a web portal to facilitate cross-species inferences about protein architecture and function in plants. PLoS One. 2013; 8(12):e82569. PMC: 3858315. DOI: 10.1371/journal.pone.0082569. View

15.

Bullard J, Purdom E, Hansen K, Dudoit S . Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics. 2010; 11:94. PMC: 2838869. DOI: 10.1186/1471-2105-11-94. View

16.

Sekhon R, Lin H, Childs K, Hansey C, Buell C, de Leon N . Genome-wide atlas of transcription during maize development. Plant J. 2011; 66(4):553-63. DOI: 10.1111/j.1365-313X.2011.04527.x. View

17.

Berthet S, Demont-Caulet N, Pollet B, Bidzinski P, Cezard L, Le Bris P . Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell. 2011; 23(3):1124-37. PMC: 3082258. DOI: 10.1105/tpc.110.082792. View

18.

Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C . Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell. 2006; 18(11):3252-74. PMC: 1693956. DOI: 10.1105/tpc.106.042689. View

19.

Ioannidis N, Cruz J, Kotzabasis K, Kramer D . Evidence that putrescine modulates the higher plant photosynthetic proton circuit. PLoS One. 2012; 7(1):e29864. PMC: 3257247. DOI: 10.1371/journal.pone.0029864. View

20.

Nylander M, Heino P, Helenius E, Palva E, Ronne H, Welin B . The low-temperature- and salt-induced RCI2A gene of Arabidopsis complements the sodium sensitivity caused by a deletion of the homologous yeast gene SNA1. Plant Mol Biol. 2001; 45(3):341-52. DOI: 10.1023/a:1006451914231. View