Different Hormonal Regulation of Cellular Differentiation and Function in Nucellar Projection and Endosperm Transfer Cells: a Microdissection-based Transcriptome Study of Young Barley Grains

Overview

Journal Plant Physiol

Specialty Physiology

Date 2008 Sep 12

PMID 18784282

Citations 52

Authors

Johannes Thiel

Diana Weier

Nese Sreenivasulu

Marc Strickert

Nicola Weichert

Michael Melzer

Tobias Czauderna

Ulrich Wobus

Hans Weber

Winfriede Weschke

Affiliations

Soon will be listed here.

Abstract

Nucellar projection (NP) and endosperm transfer cells (ETC) are essential tissues in growing barley (Hordeum vulgare) grains, responsible for nutrient transfer from maternal to filial tissues, endosperm/embryo nutrition, and grain development. A laser microdissection pressure catapulting-based transcriptome analysis was established to study NP and ETC separately using a barley 12K macroarray. A major challenge was to isolate high-quality mRNA from preembedded, fixed tissue while maintaining tissue integrity. We show that probes generated from fixed and embedded tissue sections represent largely the transcriptome (>70%) of nonchemically treated and nonamplified references. In NP, the top-down gradient of cellular differentiation is reflected by the expression of C3HC4-type ubiquitin ligases and different histone genes, cell wall biosynthesis and expansin/extensin genes, as well as genes involved in programmed cell death-related proteolysis coupled to nitrogen remobilization, indicating distinct areas simultaneously undergoing mitosis, cell elongation, and disintegration. Activated gene expression related to gibberellin synthesis and function suggests a regulatory role for gibberellins in establishment of the differentiation gradient. Up-regulation of plasmalemma-intrinsic protein and tonoplast-intrinsic protein genes indicates involvement in nutrient transfer and/or unloading. In ETC, AP2/EREBP-like transcription factors and ethylene functions are transcriptionally activated, a response possibly coupled to activated defense mechanisms. Transcriptional activation of nucleotide sugar metabolism may be attributed to ascorbate synthesis and/or cell wall biosynthesis. These processes are potentially controlled by trehalose-6-P synthase/phosphatase, as suggested by expression of their respective genes. Up-regulation of amino acid permeases in ETC indicates important roles in active nutrient uptake from the apoplastic space into the endosperm.

Citing Articles

Transport and spatio-temporal conversion of sugar facilitate the formation of spatial gradients of starch in wheat caryopses.

Zhong Y, Chen Y, Pan M, Li X, Hebelstrup K, Cai J Commun Biol. 2024; 7(1):928.

PMID: 39090206 PMC: 11294588. DOI: 10.1038/s42003-024-06625-4.

Dissection of Developmental Programs and Regulatory Modules Directing Endosperm Transfer Cell and Aleurone Identity in the Syncytial Endosperm of Barley.

Hertig C, Rutten T, Melzer M, Schippers J, Thiel J Plants (Basel). 2023; 12(8).

PMID: 37111818 PMC: 10142620. DOI: 10.3390/plants12081594.

SWEET11b transports both sugar and cytokinin in developing barley grains.

Radchuk V, Belew Z, Gundel A, Mayer S, Hilo A, Hensel G Plant Cell. 2023; 35(6):2186-2207.

PMID: 36857316 PMC: 10226576. DOI: 10.1093/plcell/koad055.

Immunocytochemical Analysis of the Wall Ingrowths in the Digestive Gland Transfer Cells in L. (Droseraceae).

Plachno B, Kapusta M, Stolarczyk P, Swiatek P, Strzemski M, Miranda V Cells. 2022; 11(14).

PMID: 35883661 PMC: 9322817. DOI: 10.3390/cells11142218.

Laser microdissection transcriptome data derived gene regulatory networks of developing rice endosperm revealed tissue- and stage-specific regulators modulating starch metabolism.

Ishimaru T, Parween S, Saito Y, Masumura T, Kondo M, Sreenivasulu N Plant Mol Biol. 2022; 108(4-5):443-467.

PMID: 35098404 PMC: 8894313. DOI: 10.1007/s11103-021-01225-w.

References

Tsujimoto Y, Shimizu S . The voltage-dependent anion channel: an essential player in apoptosis. Biochimie. 2002; 84(2-3):187-93. DOI: 10.1016/s0300-9084(02)01370-6. View

Ostersetzer O, Adam Z . Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: the possible role of the FtsH protease. Plant Cell. 1997; 9(6):957-65. PMC: 156970. DOI: 10.1105/tpc.9.6.957. View

Liu Y, Koornneef M, Soppe W . The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell. 2007; 19(2):433-44. PMC: 1867323. DOI: 10.1105/tpc.106.049221. View

Keller R, Renz F, Kossmann J . Antisense inhibition of the GDP-mannose pyrophosphorylase reduces the ascorbate content in transgenic plants leading to developmental changes during senescence. Plant J. 1999; 19(2):131-41. DOI: 10.1046/j.1365-313x.1999.00507.x. View

Stone S, Callis J . Ubiquitin ligases mediate growth and development by promoting protein death. Curr Opin Plant Biol. 2007; 10(6):624-32. DOI: 10.1016/j.pbi.2007.07.010. View

Woll K, Borsuk L, Stransky H, Nettleton D, Schnable P, Hochholdinger F . Isolation, characterization, and pericycle-specific transcriptome analyses of the novel maize lateral and seminal root initiation mutant rum1. Plant Physiol. 2005; 139(3):1255-67. PMC: 1283763. DOI: 10.1104/pp.105.067330. View

Radchuk V, Borisjuk L, Radchuk R, Steinbiss H, Rolletschek H, Broeders S . Jekyll encodes a novel protein involved in the sexual reproduction of barley. Plant Cell. 2006; 18(7):1652-66. PMC: 1488922. DOI: 10.1105/tpc.106.041335. View

Thompson R, Hueros G, Maitz M . Development and functions of seed transfer cells. Plant Sci. 2001; 160(5):775-783. DOI: 10.1016/s0168-9452(01)00345-4. View

Vierstra R . The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 2003; 8(3):135-42. DOI: 10.1016/S1360-1385(03)00014-1. View

10.

Hueros G, Royo J, Maitz M, Salamini F, Thompson R . Evidence for factors regulating transfer cell-specific expression in maize endosperm. Plant Mol Biol. 1999; 41(3):403-14. DOI: 10.1023/a:1006331707605. View

11.

Elkeles A, Devos K, Graur D, Zizi M, Breiman A . Multiple cDNAs of wheat voltage-dependent anion channels (VDAC): isolation, differential expression, mapping and evolution. Plant Mol Biol. 1995; 29(1):109-24. DOI: 10.1007/BF00019123. View

12.

Sun X, Peng L, Guo J, Chi W, Ma J, Lu C . Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell. 2007; 19(4):1347-61. PMC: 1913764. DOI: 10.1105/tpc.106.049510. View

13.

Serna A, Maitz M, OConnell T, Santandrea G, Thevissen K, Tienens K . Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. Plant J. 2001; 25(6):687-98. DOI: 10.1046/j.1365-313x.2001.01004.x. View

14.

Jauh G, Fischer A, Grimes H, Ryan Jr C, Rogers J . delta-Tonoplast intrinsic protein defines unique plant vacuole functions. Proc Natl Acad Sci U S A. 1998; 95(22):12995-9. PMC: 23684. DOI: 10.1073/pnas.95.22.12995. View

15.

Laux T, Jurgens G . Embryogenesis: A New Start in Life. Plant Cell. 1997; 9(7):989-1000. PMC: 156973. DOI: 10.1105/tpc.9.7.989. View

16.

Alboresi A, Gestin C, Leydecker M, Bedu M, Meyer C, Truong H . Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant Cell Environ. 2005; 28(4):500-12. DOI: 10.1111/j.1365-3040.2005.01292.x. View

17.

Wheeler D, Newbigin E . Expression of 10 S-class SLF-like genes in Nicotiana alata pollen and its implications for understanding the pollen factor of the S locus. Genetics. 2007; 177(4):2171-80. PMC: 2219507. DOI: 10.1534/genetics.107.076885. View

18.

Sreenivasulu N, Altschmied L, Radchuk V, Gubatz S, Wobus U, Weschke W . Transcript profiles and deduced changes of metabolic pathways in maternal and filial tissues of developing barley grains. Plant J. 2004; 37(4):539-53. DOI: 10.1046/j.1365-313x.2003.01981.x. View

19.

Borisjuk L, Wang T, Rolletschek H, Wobus U, Weber H . A pea seed mutant affected in the differentiation of the embryonic epidermis is impaired in embryo growth and seed maturation. Development. 2002; 129(7):1595-607. DOI: 10.1242/dev.129.7.1595. View

20.

Runeberg-Roos P, Tormakangas K, Ostman A . Primary structure of a barley-grain aspartic proteinase. A plant aspartic proteinase resembling mammalian cathepsin D. Eur J Biochem. 1991; 202(3):1021-7. DOI: 10.1111/j.1432-1033.1991.tb16465.x. View