Research Group Hochholdinger

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PD Dr. Frank Hochholdinger

ZMBP, Allgemeine Genetik
Universität Tübingen
Auf der Morgenstelle 28
D-72076 Tübingen
Germany

Tel. +49-7071 / 29 77 0 24
Fax. +49-7071 / 29 50 42
e-mail: frank.hochholdinger(at)zmbp.uni-tuebingen.de

PD Dr. Frank Hochholdinger

 


 


Research Interests
Genetic analysis of root formation in maize (Zea mays)

Root systems of terrestrial plants serve many important tasks among which anchorage as well as water and nutrient intake are the most important ones. Cereals including maize (Zea mays) account for about 70% of the human calorie uptake worldwide. Despite their agronomic importance a systematic genetic analysis of root formation in cereals has only recently been initiated. The root system of maize can be divided into an embryonic root system consisting of a single primary root and a variable number of seminal roots and a post-embryonic root system which is made up by shoot-borne roots formed at consecutive under and aboveground nodes. Lateral roots which emerge from all major root-types also belong to the post-embryonic root system.

Major root types of maize

Differences between the root systems of cereals and Arabidopsis

 

Cereals

Arabidopsis

Morphology

 

 

Embryonic root system

primary root + seminal roots (in maize)

primary root

Shoot-borne root system

extensive

missing

Anatomy

 

 

Cell-types forming lateral roots

pericycle and endodermis

pericycle

Number of cortical cell-layers

10-15

1

Number of cortical cells (transverse)

variable

8

Number of quiescent center cells

800-1200

4

Number of root initial cells

few

several hundred

 

Mutant analysis of maize root formation

Recently, we have identified a number of monogenic recessive mutants specifically affected in various aspects of shoot-borne and lateral root formation.

Shoot-borne roots make up the major backbone of the maize root system and are unique to cereals. Therefore, we are particularly interested in this root-type and were able to identify a mutant (rtcs) specifically affected in shoot-borne root initiation. After cloning of the rtcs gene which encodes for a lob domain transcription factor a functional characterization of this gene and its interactions is under way.

In maize, genetic evidence suggests that at least two distinct pathways control lateral root initiation in embryonic and postembryonic roots. This notion is supported by the identification of mutants that are specifically affected in lateral root formation of the embryonic roots while lateral root formation in the postembryonic root system is not affected. In addition to several lateral root mutants which we have characterized previously we have recently identified a novel mutant rum1, which is specifically affected in the initiation of seminal roots and lateral roots in the primary root. The reduced auxin transport and delayed gravitropism of that mutant suggests that the affected gene might be involved in auxin mediated initiation of the affected roots.

Our laboratory is also involved in a co-operative project with the goal of functionally characterizing two recently cloned root hair mutants of maize encoding for a sec3 homolog (rth1) and a phytochelatine synthase (rth3).

Characteristics of monogenic maize root mutants

Affected root-type

Mutant name

Reference

Affected phase of root development

Affected phase of the root system development

Mutagen

Shoot-borne roots

rtcs

Hetz et al., (1996)

Initiation

Late embryonic and late postembryonic

Transposon (En/Spm)

rt1

Jenkins, (1930)

Late postembryonic

Unknown

Lateral roots

rum1

Woll et al., (2005)

Late embryonic and early postembryonic

Transposon (Mu)

lrt1

Hochholdinger and Feix, (1998)

Early postembryonic

EMS

slr1

Hochholdinger et al., (2001)

Elongation

Transposon (Mu)

slr2

Root hairs

rth1

Wen and Schnable, (1994)

Wen et al., (2005)

Differentiation

Embryonic and postembryonic

rth2

rth3

 

Reverse genetic analysis of maize root formation

In addition to the characterization of novel root mutants of maize and the cloning of the affected genes we are utilizing these specific mutants for high throughput microarray and proteome analyses. The goal of these studies is to better understand the molecular networks that are active during the early stages of maize root formation and to identify genes and proteins that are differentially expressed between wild-type and mutant genotypes. Such genes might be downstream regulators of the mutated genes and are the starting point of reverse genetic studies, which aim on the knock out of these genes and the subsequent functional characterization of these novel mutants.

Recently, we have extended our microarray analyses to cell-type specific gene expression studies by combining laser capture microdissection with microarray hybridizations.

Proteomics combines the resolution of 2-D gel electrophoresis with the sensitivity of mass spectrometry. On the proteome level we studied various aspects of maize root formation including lateral and shoot-borne root initiation and the early proteome changes during primary root development .

Manifestation of heterosis in seedling roots

Heterosis is a phenomenon that describes the superior performance of F1-hybrids over their homozygous parental inbred lines. Typically heterosis is measured in terms of increased yield or vigour. However, heterosis is already manifested during early seedling development and can be measured as increased primary root length, cortical cell length or lateral root density. Therefore we chose the young maize seedling root system as a model to study the early molecular events leading to heterosis. Currently we compare the gene expression patterns of four local maize inbred lines and their reciprocal hybrids in an extensive microarray analysis. Subsequently, differentially expressed genes will be functionally characterized and their allelic contribution to gene expression will be determined.


Kompetenzzentren Life Sciences

The Schwechheimer and Hochholdinger labs of the ZMBP participate in the "Kompetenzzentren LifeSciences" project. Objective of this project is to provide high school students and teachers with a basic background in molecular biology. Currently we establish a novel trimodular training program that combines aspects of genetic, bioinformatic and molecular analyses. The experiments of the first two modules can be performed at home or in school, the third modul is a one day training in molecular biology at the University of Tübingen.



Publications

 

 

 

 

2010

 

Ma W., Muthreich N., Liao C., Franz-Wachtel M., Schütz W., Zhang F., Hochholdinger F., Li C. (2010): The mucilage proteome of maize (Zea mays L.) primary roots. J Proteome Res., in press, PMID: 20408568.

Zimmermann R., Sakai H., Hochholdinger F. (2010): The Gibberelic Acid Stimulated Like (GSL) gene family in maize (Zea mays L.) and its role in lateral root development. Plant Physiol., 152: 356-365.

Saleem M., Lamkemeyer T., Schutzenmeister A., Madlung J., Sakai H., Piepho H.P., Nordheim A., Hochholdinger F. (2010): Specification of cortical parenchyma and stele of maize (Zea mays L.) primary roots by asymmetric levels of auxin, cytokinin and cytokinin-regulated proteins.  Plant Physiol., 152: 4-18.   

Muthreich N., Schützenmeister A., Schütz W., Madlung J., Krug K., Nordheim A., Piepho H.-P., Hochholdinger F. (2010): Regulation of the maize (Zea mays L.) embryo proteome by RTCS which controls seminal root initiation. Eur. J. Cell Biol., 89: 242-249.   

Liu Y., von Behrens I., Muthreich N., Schütz W., Nordheim A., Hochholdinger F. (2010): Regulation of the pericycle proteome in maize (Zea mays L.) primary roots by RUM1 which is required for lateral root initiation. Eur. J. Cell Biol., 89: 236-241.   

Paschold A., Marcon C., Hoecker N., Hochholdinger F. (2010): Molecular dissection of heterosis manifestation during early maize root development. Theor. Appl. Genet. 120: 383-388.

 

2009

Saleem M., Lamkemeyer T., Schuetzenmeister A., Fladerer C., Piepho H.-P., Nordheim A., Hochholdinger F. (2009): Tissue specific control of the maize (Zea mays L.) embryo, cortical parenchyma, and stele proteomes by RUM1 which regulates seminal and lateral root initiation. J. Proteome Res. 8: 2285-2297.

Hochholdinger F., Zimmermann R. (2009): Molecular and genetic dissection of cereal root development. Ann. Plant Rev. 37: 175–191 (invited review).

Hochholdinger F. (2009): The Maize Root System: Morphology, Anatomy and Genetics. In The Handbook of Maize (eds J. Bennetzen, S. Hake) pp. 145-160. Springer, New York, Inc

Hochholdinger F., Tuberosa R. (2009): Genetic and genomic dissection of maize root development and architecture. Curr. Opin. Plant Biol. 12: 172-177.

2008

Hoecker N., Lamkemeyer T., Sarholz B., Paschold A., Fladerer C., Madlung J., Wurster K., Stahl M., Piepho H.-P., Nordheim A., Hochholdinger F. (2008): Analysis of non-additive protein accumulation in young primary roots of a maize (Zea mays L.) F1-hybrid compared to its parental inbred lines. Proteomics 8: 3882–3894.

Hoecker N., Keller B., Muthreich N., Chollet D., Descombes P., Piepho H.-P., Hochholdinger F. (2008): Comparison of maize (Zea mays L.)  F1-hybrid and parental inbred line primary root transcriptomes suggests organ specific patterns of non-additive gene expression and conserved expression trends between different hybrids. Genetics 179: 1275-83.

Hala M., Cole R., Synek L., Drdova E., Pecenkova T., Nordheim A., Lamkemeyer T., Madlung J., Hochholdinger F., Fowler J.E., Zarsky V. (2008): An exocyst complex functions in plant cell growth. Plant Cell 20: 1330-45.

Hochholdinger F.*, Wen T.J.*, Zimmermann R., Chimot-Marolle P., da Costa e Silva O., Bruce W., Lamkey K.R., Wienand U., Schnable P.S. (2008): The maize (Zea mays L.) roothairless3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield. Plant J. 54: 888-98. * Co-first authors

Hochholdinger F., Zimmermann R. (2008): Conserved and diverse mechanisms in root development. Curr. Opin. Plant Biol. 11: 70-74.

2007

Dembinsky D., Woll K., Saleem M., Liu Y., Fu Y., Borsuk L.A., Lamkemeyer T., Fladerer C., Madlung J., Barbazuk B., Nordheim N., Nettleton D., Schnable P.S., Hochholdinger F. (2007): Transcriptomic and proteomic analyses of pericycle cells of the maize (Zea mays L.) primary root. Plant Physiol.145: 575-588.

Hochholdinger F., Hoecker N. (2007): Towards the molecular basis of heterosis. Trends Plant Sci. 12: 427-432.

Taramino G., Sauer M., Stauffer J., Multani D., Niu X., Sakai H., Hochholdinger F. (2007): The rtcs gene in maize (Zea mays L.) encodes a lob domain protein that is required for postembryonic shoot-borne and embryonic seminal root initiation. Plant J. 50: 649-659.

Hochholdinger F. (2007): Genetische Analyse der Wurzelentwicklung von Mais (Zea mays L.): Von Mutanten zu Genen, Transkriptomen und Proteomen. Beiträge zur Hallenser Pflanzenernährungsforschung 14: 16-20.

2006

Liu Y., Lamkemeyer T., Jakob A., Mi G., Zhang F., Nordheim A., Hochholdinger F. (2006): Comparative proteome analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1. Proteomics, 6: 4300-4308.

Woll K., Dressel A., Sakai H., Piepho H.-P., Hochholdinger F. (2006): The root tip specific gene ZmGrp3: A novel marker for root initiation and a model to study allelic contribution to gene expression in maize (Zea mays L.) primary roots. Theor. Appl. Genet. 113: 1305-1315.

Sauer M., Jakob A., Nordheim A., Hochholdinger F. (2006): Proteomic analysis of shoot-borne root initiation in maize (Zea mays L.). Proteomics 6: 2530-2541.

Hoecker N., Keller B., Piepho H.-P., Hochholdinger F. (2006): Manifestation of heterosis during early maize (Zea mays L.) root development. Theor. Appl. Genet. 112: 421-429.

Piepho H.P., Keller B., Hoecker N., Hochholdinger F. (2006): Combining signals from spotted maize (Zea mays L.) cDNA microarrays obtained at different scanning intensities. Bioinformatics 22: 802-807.

Hochholdinger F., Sauer M., Dembinsky D., Hoecker N., Muthreich N., Saleem M., Liu Y. (2006): Proteomic dissection of plant development. Proteomics 6: 4076-4083.

Schlicht M., Strnad M., Scanlon M., Mancuso S., Hochholdinger F., Palme K., Volkmann D., Menzel D., Baluska F. (2006): Auxin Enrichment at Actin-Based Synapses and within Adjacent Endosomes Implicate Vesicular Neurotransmitter-Like Mode of Polar Auxin Transport in Root Apices. Plant Signaling and Behaviour 1:122-133.

2005

Hochholdinger F., Woll K., Sauer M., Feix G. (2005): Functional genomic tools in support of the genetic analysis of root development in maize (Zea mays L.). 50th anniversary edition of Maydica 50: 437-442.

Woll K., Borsuk L., Stransky H., Nettleton D., Schnable P.S., Hochholdinger F. (2005): Isolation, characterization and pericycle specific transcriptome analyses of the novel maize (Zea mays L.) lateral and seminal root initiation mutant rum1. Plant Physiol. 139: 1255-1267.

Hochholdinger F., Woll K., Guo L., Schnable P.S. (2005): Analysis of the soluble proteome of maize (Zea mays L.) primary roots reveals drastic changes in protein composition during early development. Proteomics 18: 4885-4893.

Wen T.J.*, Hochholdinger F.*, Sauer M., Bruce W., Schnable P.S. (2005): The roothairless1 gene of maize (Zea mays) encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol. 138: 1637-1643. * Co-first authors

Keller B., Emrich K., Hoecker N., Sauer M., Hochholdinger F., Piepho H.-P. (2005): Designing a Microarray Experiment to Estimate Dominance in Maize (Zea mays). Theor Appl Genet. 111: 57-64.

Jung S., Hwang I., Hochholdinger F., Oh Y.J., Lee Y., Eun M.Y., Park W.J. (2005): Progress in the genetic studies on root development in Oryza sativa. J Nano Bio Tech. 2:66-70.

Hoecker N., Hochholdinger F. (2005): Morphological characterization of heterotic traits in early root development of maize. Maize Genet. Coop. Newsletter 79: 44-45.

2004

Hochholdinger F., Guo L., Schnable P.S. (2004): Cytoplasmic regulation of the accumulation of nuclear-encoded proteins in the mitochondrial proteome of maize. Plant J. 37(2): 199-208.

Schnable P.S., Hochholdinger F., Nakazono M. (2004): Global Expression Profiling Applied to Plant Development. Current Opin Plant Biol. 7(1): 50-56.

Hochholdinger F., Woll K., Sauer M., Dembinsky D. (2004): Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programs. Annals Bot. 93: 359-368.

Park W.J., Hochholdinger F., Gierl A. (2004): Release of defense molecules the benzoxazinoids during lateral- and crown root emergence in Zea mays. J Plant Physiol. 161: 981-985.

Hochholdinger F., Guo L., Schnable P.S. (2004): Lateral roots affect the proteome of the primary root of maize (Zea mays L.). Plant Mol Biol. 56: 397-412.

Hochholdinger F., Park W.J., Sauer M., Woll K. (2004): From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci. 9: 42-48.

Woll K., Hochholdinger F. (2004): Isolation of a new root mutant affected in lateral and seminal root initiation. Maize Genet. Coop. Newsletter 78: 59-60.

Before 2004

Woll K., Hochholdinger F. (2003): ZmGrp3 is exclusively expressed in epidermal cells of the root tip and the columella. Maize Genet. Coop. Newsletter 77: 73.

Feix G., Hochholdinger F., Park W.J. (2002): Maize root system and Genetic Analysis of ist formation. In Plant roots the hidden half. 3rd ed. (eds Y. Waisel, A. Eshel and U. Kafkafi) pp. 239-248. Marcel Dekker, New York, Inc

Hochholdinger F.*, Park W.-J.*,Feix G. (2001): Cooperative action of SLR1 and SLR2 is required for lateral root specific cell-elongation in maize. Plant Physiol., 125: 1529-1539. * Co-first authors

Hochholdinger F., Wulff D., Reuter K., Park W.-J., Feix G. (2000): Tissue specific expression of AUX1 in maize roots. J. Plant Physiol. 157: 315-319.

Hochholdinger F., Park W.-J., Feix G. (1999): The newly isolated root mutant slr2 is affected in lateral root elongation. Maize Genet. Coop. Newsletter 73: 32-33.

Hochholdinger F., Feix G. (1998a): Early post-embryonic root formation is specifically affected in the maize mutant lrt1. Plant J. 16: 247-255.

Hochholdinger F., Feix G. (1998b): Cyclin expression is completely suppressed at the site of crown root formation in the nodal region of the maize root mutant rtcs. J. Plant Physiol. 153: 425-429.

Hochholdinger F., Feix G. (1998c): Tiller formation in gaspe flint is not affected by the rtcs locus. Maize Genet. Coop. Newsletter 72: 30-31.

Hochholdinger F., Feix G. (1998d): Isolation of the new necrotic root mutant brt1. Maize Genet. Coop. Newsletter 72: 29-30.

Hochholdinger F., Park W.-J., and Feix G. (1998): Isolation of the new root mutant slr1 affecting lateral root formation. Maize Genet. Coop. Newsletter 72: 30.

Hochholdinger F., Schnable P., Feix G. (1997): Isolation of the new recessive mutant lrt1 deficient in lateral root formation. Maize Genet. Coop. Newsletter 71: 35.

Hetz W., Hochholdinger F., Schwall M., Feix G. (1996): Isolation and characterisation of rtcs, a mutant deficient in the formation of nodal roots. Plant J. 10: 845-857.

Hochholdinger F., Hetz W., Feix G. (1996): Juvenile-adult phase transition of vegetative traits is not affected in the root deficient mutant rtcs. Maize Genet. Coop. Newsletter 70: 23.

 


Posters

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Funding

SPP1149 Heterosis in Plants

SFB446 Mechanisms of cell behaviour in eukaryotes


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Diplomarbeiten

Wir bieten ständig Diplomarbeiten zu verschiedenen Aspekten der molekularen Analyse der Maiswurzelentwicklung an. Bei Interesse wenden Sie sich bitte an Frank Hochholdinger, Auf der Morgenstelle 28, 72076 Tübingen, 8. Ebene Raum A08, Tel. 07071 / 29 77024