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The authors reviewed the history, milestones and perspectives in plant developmental biology...

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Perspectives in plant developmental biology
- Historical perspectives on plant developmental biology

Although the survey of milestones is far from complete it is obvious that in the past 15 years a lot of progress has been made in the identification of the genetic control of pattern formation during embryogenesis, organ (leaf and flower) formation and in tissue differentiation. Many of the transcription factors involved have been cloned and studied, however much less effort was investigated so far in the study of the upstream signaling cascades and intrinsic and external stimuli that direct these patterning processes through transcription factor activation or repression (Hay et al., 2004). It will be a future challenge to link the genetics to the physiology of the plant.

A lot of research needs to be done on the communication processes between the cells of the multicellular plant as well as between its different tissues and organs. Hormones have been shown to be important to direct developmental processes at the whole organism level, but the molecular mechanism of their circulation through the plant is still poorly understood. In addition other signaling molecules have been recognized as important communicators such as small peptides, oligosaccharides and metabolites such as salicylic acid. The peptides appear to have crucial functions in tissue domain interaction such as CLV3 in the regulatory loop for self-maintenance of the SAM and in cell-cell interaction such as SCR in the self-incompatibility response (Matsubayashi, 2003). A lot of small open reading frames are out there in the genome and their function remains to be solved. The role of volatiles such as jasmonic acid in plant development needs to be further explored. The regulation of plasmodesmata formation and closure between cells and tissue domains has been shown to be important in communication and needs further attention.

Another big question to be solved is how organ size and shape are determined. Over the last years it became clear that not only cell expansion but also cell division is important. At some point in development cells in meristems need to know when to leave the cell cycle and start the differentiation process. The signals and molecular mechanisms need to be determined that control the switch between cell cycle entry and exit during development and in response to environmental cues (Gutierrez, 2005). It took a decade to functionally analyze 10% of the Arabidopsis genes using forward genetics. In the meantime large mutagenized seed collections have been generated that are exploited for reverse genetics of gene families. Within the next five years of Arabidopsis research the aim is to uncover the function of every gene; the National Science Foundation 2010 project is the leading initiative. This will be possible because there is a shift to largescale experimentation in which not a single gene but rather its whole gene family is functionally analyzed. From the genome sequence, all the members of a given gene family can be retrieved; by reverse genetics, mutations can be looked for in the available collections and be analyzed for their phenotype. The function of large gene families such as the cellulose synthase-like genes (Bonetta et al., 2002) or myb-type transcription factors (Meissner et al., 1999) are analyzed by reverse genetics. In large gene families functions might be redundant because of recent gene duplication resulting in the lack of phenotypes by single gene knockout. In order to define functions, double or even triple mutant combinations of knockouts will have to be made in the respective paralogs. A few nice examples illustrate this approach, such as for the MADS-box SEPALLATA genes (Pelaz et al., 2000) and the B-function genes in petunia (Vandenbussche et al., 2004). Unknown proteins for which a mutant phenotype has been obtained are analyzed for their interactions with other proteins by means of yeast-two-hybrid analysis or TAP tagging to get a clue to their molecular function. A number of unknown proteins identified by embryo-lethals are studied in this way (Berg et al., 2004). The wealth of information on gene function in model systems will serve to improve plant product quality and adaptation of plants to changing environments. Genes from model systems have been overexpressed in other species with success (Weigel and Nilsson, 1995); however, they mainly serve to isolate and study the orthologs in crops (Byzova et al., 2004). The synteny of large chromosomal domains between related species has been exploited to use gene knowledge obtained in model systems such as Arabidopsis for molecular breeding in related crops such as Brassica species (Lagercrantz et al., 1996). Synteny between cereal genomes is high and the rice genome sequence is used as reference to aid for instance in positional cloning of genes in maize (Devos, 2005). Quantitative trait loci analysis is an approach to identify and clone genes that contribute to complex phenotypes such as seed weight or leaf size and shape and has been successfully used in a number of plant species (Alonso- Blanco and Koornneef, 2000; Pérez-Pérez et al., 2002; Morgante and Salamini, 2003; Tanksley, 2004).

More model species for developmental studies are emerging such as Medicago truncatula to study nodule formation upon symbiosis with Sinorhizobium (Cook, 1999; Young et al., 2003) and the tree model Populus to study wood formation and, more recently, cambium activity (Bhalerao et al., 2003; Brunner et al., 2004). These model systems fulfill a number of criteria such as diploidy, easy transformation, small genome, ongoing genome sequencing, big consortia for coordinated international research and maintenance and availability of genetic resources. In this new research tendency the diversity in plant developmental processes is recognized to exceed the potential of just a few model systems. Soon there will be a shift from the model species to a wide range of species to study species-specific development or morphologies as for instance the «cluster» root (Shane et al., 2004) and to study processes for which Arabidopsis is not a good model such as for domestication, mycorrhizae interaction or nodule formation. With the increasing functional analyses of genes from model species, comparative analysis will become more important and powerful. DNA sequencing technology is automated and its efficiency has improved tremendously over the last five years, so that not the amount of work but rather the cost and bioinformatics tools will be the limiting factors for sequence analysis of a specific species in the near future (Venter, 2004). New areas of research, such as comparative genetics, will exploit this sequence information and couple it to questions related to gene function conservation or divergence. A well-studied case is the homeobox gene function divergence between plants and animals (Meyerowitz, 2002). The conclusion is that similar processes of pattern formation are used in plant and animal developmental programs; however different classes of regulatory genes have been recruited for it during evolution. Comparative genetics relies on DNA sequence information and aims at studying a genetic trait within a plant family or even between incompatible species and overcomes the genetic barrier of crossing inhibition. Another emerging field is evolutionary developmental biology the so-called “Evo-Devo” that also exploits DNA sequence information to explain morphological diversity. Function conservation of key regulators in development, such as the MADS-box transcription factors with a role in flower organ specification, begins to explain the main aspects of flower morphology in different species, such as the different floral organ types and the floral whorls. Gene duplication and function divergence by coding sequence changes in addition to ectopic expression patterns clarify the diversity in flower morphology in a number of cases (Kramer and Irish, 1999; Vandenbussche et al., 2003b; Ferrario et al., 2004). Evolutionary developmental biology studies have investigated some aspects of diversity in leaf morphology as well (Cubas et al., 1999b; Bharathan et al., 2002; Kanno et al., 2003; Hileman et al., 2003; Tsiantis and Hay, 2003). Bioinformatics research showed that diploid genomes, such as that of Arabidopsis and other model systems contain large genome duplications (Arabidopsis Genome Initiative, 2000; Simillon et al., 2002; Blanc and Wolfe, 2004). Genome duplications have been postulated to allow for diversification in gene function and to be the major mechanism to achieve morphological diversity in the flowering plants and also in the animal kingdom in combination with natural selection as postulated by C. Darwin in the late 19th century (Darwin, 1859; Ohno, 1970). Computational approaches to unveil ancient genome duplications are under development and may contribute to new insights into evolutionary genetics (Van de Peer, 2004). Significant progress in the unraveling of molecular networks is to be expected from the systems biology approach in which the entire transcriptome, proteome, or metabolome is analyzed upon perturbation rather than single genes. The aim is to identify the complex networks responsible for biological processes and their mutual interactions (Gutiérrez et al., 2005). Integration with computational science and mathematics will be indispensable to interpret the large data sets, generate network visualization and build models. The number of computer programs for visualization and integration of different data sets, such as MAPMAN (Thimm et al., 2004) is increasing and is a prerequisite to understand the biology. The integration of biological data into regulatory networks will allow further testing and predictions (Ideker et al., 2001; Davidson et al., 2002). Models on plant growth and development are being generated for plant architecture, organs and tissues and incorporating genetic regulatory networks. These models are an integration of mathematical modeling and computer simulations with biological components such as modules for architecture, growth parameters for organs and tissues, or genes and their domains of action and genetic interaction for regulatory networks (Rolland-Lagan et al., 2003; Kwiatkowska and Dumais, 2003; Gielis, 2003; Prusinkiewicz, 2004). Future goals are the integration of models for architecture with those for organs and tissues and for genetic regulatory networks in order to obtain in-depth understanding of the mechanisms of plant development from genes to phenotypes (Prusinkiewicz, 2004).

Plant cell sorting has recently been achieved by several groups to purify living cells of the same type with cell-specific GFP markers, or alternatively small tissue domains with laser technology (Kerk et al., 2003; Birnbaum et al., 2003). Plant cell sorting is a breakthrough technology since research on cell differentiation in plants was limited to molecular-genetic analysis because of the inability to culture differentiated plant cells in vitro unlike in mammalian systems. The genome-wide profiling techniques are applied to this sorted plant material and the results will undoubtedly further our knowledge on the progressive process of cell specification to differentiation and cell function. Increasing the resolution of sorting and systems biology up to single cell level will open up new opportunities in the study of cell specification. Then, genetic programs would be analyzed that distinguish, for instance, between the different fate of the daughter cells after asymmetric cell division, such as in the case of the first zygotic division or upon lateral root induction or in stomatal development. Another challenge for future research on plant development will be to understand other mechanisms besides the transcriptional control of genetic programs exerted by transcription factors. Recently, microRNAs have been discovered in plants and a number of them are complementary to transcription factors with a function in developmental processes (Reinhart et al., 2002; Rhoades et al., 2002; Bonnet et al., 2004). For instance in leaf development several transcription factors, such as PHABULOSA, PHAVOLUTA and CINCINNATA -like genes are targeted by miRNAs (Nath et al., 2003; Palatnik et al., 2003; Juarez et al., 2004; Kidner and Martienssen 2004). Temporal and spatial regulation of expression of miRNAs is of utmost importance for the proper destruction of transcription factor mRNAs during developmental processes and it is based on the silencing pathway (Baulcombe, 2004). However, the regulation of expression of the miRNAs is still unknown and needs to be explored because it adds another level to gene expression regulation and it may contribute to the delineation of boundaries and domains in developing organisms.

Protein degradation through the ubiquitination pathway is an important control mechanism for developmental pathways. E3 ubiquitin ligases target specific substrates for degradation at the proteasome and more than 460 are represented in the Arabidopsis genome (Stone et al., 2005). A number of their targets will be important in developmental control and their nature will be revealed in the coming years by functional genomics. Epigenetic control of developmental transitions and morphogenetic processes needs to be further explored (Reyes et al., 2002). The naturally occurring peloric mutant of Linaria vulgaris described by Linnaeus more than 250 years ago has an epigenetic mutation in a CYC ortholog (Linneaus, 1749; Gustafsson, 1979; Cubas et al., 1999b). Other well-studied epimutations are at the P locus in maize and at the SUPERMAN locus in Arabidopsis (Das and Messing, 1994; Jacobsen and Meyerowitz, 1997). From these studies it became clear that the DNA methylation status has a great impact on gene expression and can be transferred to subsequent generations in plants. As mentioned, the DRL1 and ELO genes studied in our unit (Nelissen et al., 2003, 2005) identified a histone acetyltransferase complex, named Elongator that associates with the RNA polymerase II transcription elongation complex. The drl1-2 and elo mutants have a narrow leaf phenotype indicating that leaf form is also regulated by reversible chromatin modification. The drl1-2 and elo mutants have in addition reduced root growth, a stunted inflorescence and an altered phyllotaxis (Figure 2). Reversible histone modifications,such as acetylation/deacetylation, are of critical importance to make DNA available for transcription or to repress transcription. A well-studied case is the vernalization-dependent deacetylation and, hence, inactivation of the FLOWERING LOCUS C gene that codes for a repressor of flowering (Sung and Amasino, 2004). A number of histone acetylases and deacetylases (HDAC) are present in the plant genome, amongst them the plant-specific HD2 subfamily of HDACs (Lusser et al., 1997; Pandey et al., 2002). It will be a challenge to find out about their upstream signaling, downstream targets and function in plant development. On the longer term, more than 10 years from now, it is difficult to predict the future because a major input of technology and expertise from other disciplines in biological research is to be expected. The biology-driven research relies to a great extent on breakthrough technologies to take the research to the next level. No doubt, technology will have a huge impact on experimentation and thinking in biological research in the next decade.

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