Model plants, with special emphasis on Arabidopsis thaliana, and crop improvement

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1 Model plants, with special emphasis on Arabidopsis thaliana, and crop improvement RICHARD FLAVELL Ceres, Inc., Thousand Oaks, California 91320, USA Corresponding author: Abstract The frontiers of plant science, like the other branches of the life sciences, have been dominated by genomics over the past 25 years. This was facilitated by seminal progress in DNA manipulation developed in bacteria, bacteriophage and yeast and the fruits of the biotechnology industries that have provided DNA manipulation and sequencing technologies. Within plant genomics the functional genomics of Arabidopsis have dominated the scene in addition to provision of DNA sequences for the construction of molecular maps for many species. More is now known about Arabidopsis than any other plant. Its use as an organism for discovery in molecular genetics is based on the attributes that led to its selection for study. However, its use as a model for crops is very promising but still inadequately tested. More use of Arabidopsis (and other models) closely associated with crop breeding programs could provide a winning combination. It would enable many more hypotheses to be tested than is possible in crops and so enable better solutions for crop problems to be found. The need for improvements in all crops is so urgent that the closer association of Arabidopsis and expanded crop biology programs needs to be seriously explored and implemented where appropriate. This should be a major concern for the scientific community, funding agencies and societies at large. Perhaps the future health of our planet may, to some extent, depend on such an association. Introduction The need to produce better plants to improve and sustain quality of life for all is now more pressing than ever. The arguments are many and varied but irrefutable. It is fortunate for all societies that the urgent needs to produce sustainably more food, feed, fiber, chemicals, drugs and energy from plants are accelerating at the same time that the tools for improving crops have advanced rapidly and the knowledge base underlying plant improvement is undergoing unprecedented expansion. Tuberosa R., Phillips R.L., Gale M. (eds.), Proceedings of the International Congress In the Wake of the Double Helix: From the Green Revolution to the Gene Revolution, May 2003, Bologna, Italy, , 2005 Avenue media, Bologna, Italy.

2 This all stems from the discoveries of the structure of DNA in 1953 and all the information that has been learnt about the molecular genetics of plants as a consequence. The expansion has been particularly dramatic over the past 20 years. It is extraordinary to think that man has been selecting improved plants for over 10,000 years but only now are we reaching the point where we can start to do this in a directed way. With all the new tools and understanding that have come from studies into DNA of many organisms it is constantly relevant to ask the question have we got the crop improvement strategies right, based on the new, DNA-based knowledge, to be most cost- and time- effective and tuned optimally to meet the needs of societies? The question is crucial because societies need and expect more from plant science if qualities of life worldwide are not to be eroded in the coming decades. There are many aspects to this question and one of them surrounds the use of model species for discoveries that are needed to underpin rapid improvements in plant breeding. This article seeks to highlight the necessity of both making discoveries in model plants like Arabidopsis and using the resulting information efficiently in plant improvement programs. Challenges priorities and opportunities Investments in plant science R&D in Europe and the US have always been dwarfed by the investments in medical research. This situation has been based, presumably, on the premise that the medical needs (and curiosity) of man are far more significant and important. There is a strong case for this but all too often the case for plant science research is weakly presented and understood. Plants, after all, are sessile individuals with no brain and have no apparent communication skills. They are subservient to man and those of us who have enough food to eat have no apparent reason to improve or understand them. The large shift of people away from the land to cities in the industrialized countries over the past century has exacerbated this ignorance of plants and their role. Farmers and rural people, however, know the value of plants for survival. Is it now time for governments and the ordinary inhabitants of the world to rethink priorities. The following are facts of such magnitude that they cannot be ignored: (1)The planet needs to produce much more food to feed another 2 or 3 billion people and this must originate as plant material from many species. There is essentially no more productive land and so plant productivity has to increase substantially. Furthermore, water is getting scarce in many parts of the world and existing plant productivity is therefore more at risk. Climate changes also exacerbate stability of water supply and sustainability of crop yields. (2)Oil is becoming more expensive and likely to continue to do so as demand for it becomes greater in the developing countries where the population increases 366

3 are occurring, along with rising standards of living and industrialization. Therefore, renewable energy resources will be needed. Perhaps one day, ways of producing hydrogen fuel will be simplified and cost-effective but in the meantime, plants appear to be the best additional source of renewable energy for fuels that can be used around the world. If so, land must be found to bear very effective biomass production with low inputs. (3)As we burn fossil fuels, including coal, the concentration of CO 2 in the atmosphere is rising and this contributes to global warming that can have catastrophic consequences for some countries. Plants on the other hand, absorb CO 2 in photosynthesis and so provide carbon-neutral energy sources. They can also trap the carbon in long-lived molecules. Development of more intense plant production to provide sources of energy and transportation fuel is therefore desirable. (4)The environments everywhere must be kept in a condition that maintains plant productivity sustainable. If this fails, then future generations can rightly fear the consequences. Plant life, properly managed, helps sustain the productivity of land. As governments and societies grapple with these major issues the value of plants to our present and future will surely become more obvious to opinion-formers and decision-makers. Investment in plant research and agriculture should therefore follow to help secure the future of a healthy planet. How are the plant breeding and science communities placed to respond to such a call to help meet some global needs via better plants? Are priorities and technologies sufficiently well-developed to deliver to society what will be expected? This question has a global perspective because, in contrast to the R&D and manufacture of pills or vaccines for combatting human disease, all the species and varieties of plants required cannot be grown in a few places and shipped to where needed. Plants suited to particular climates, environments and cultures are needed and so must be evaluated in all the relevant environments where they will be grown. Thus the nature of plant science R&D and agriculture in all regions of the world must be considered. For plant breeding and science to respond rapidly to the needs of societies globally, a strong knowledge base and diverse well-trained work forces are required. In some places they have been strengthened recently while in others they have declined. In the USA and Europe training of plant field geneticists and breeders has declined considerably in favor of the molecular, laboratory-based, basic research. This is understandable but does not bode well for the future agricultural applications of all the new, DNA-based knowledge gained over the past 20 years. Realizing the value of these advances to mankind is essential and cannot be over-emphasized. Prior to the 1980s, the plant research communities were focused on making primary discoveries in a large range of species. There was much apparent duplication of discovery as the same processes were studied in multiple crop species and other 367

4 species of particular interest. This meant that progress in understanding the intricacies of many plant processes was slow and diffuse. European funding agencies were criticized for supporting research on too many species. During the 1980s, there was much debate in Europe, the USA and Australia about the value of a model species but the arguments became very strong when it was perceived that it would become possible 1) to sequence representatives of all the genes of a plant species with a small genome using technology developed for species in other kingdoms including man and 2) to study the function of every gene following saturation mutagenesis, as was being done in yeast, drosophila and C. elegans (Meyerowitz 1989; Somerville 1989). Some desirable research features required ideally of a model species for crop improvement are listed in Figure 1A. The weed Arabidopsis thaliana, studied for several decades by George Redei at the University of Missouri amongst others, became the leading candidate and is now, some 20 years later, the plant about which we know most an extraordinary phenomenon (Somerville and Koornneef 2002). It now serves as the reference higher plant. The convenience of using Arabidopsis in small university departments, with its small size, diploid genetics, small genome and relatively short generation time (in contrast to large genome, long generation crop plants), led many talented leaders to become attracted to plant science who otherwise would not have done so. This was a huge spin-off benefit from choosing a model that enabled scientific rewards to materialize rapidly and thus supported the career advancement of the most ambitious. Arabidopsis, a dicot, was chosen as the principal model, presumably because as a model now reference it was believed that the information gained on the species would be applicable to all/most higher plant species and especially the major crops of the world, in spite of many of the world s staple crops being Figure 1A. Desirable research features for a model. Figure 1B. Advantages in using a model for crop improvement. 368

5 monocots. This belief was based on the principles of evolution - that underlying all the diversity in the plant kingdom is a conserved genetic, developmental and physiological framework that can be understood from studying any species. Comparative genomics and genetics, now beginning to develop rapidly, are providing convincing evidence that this belief is scientifically correct (Izawa et al. 2003; Ware and Stein 2003; Irish and Benfey 2004; Rensink and Buell 2004). It was also envisaged that using a model species, with which it is possible to make discoveries faster and test hypotheses more rapidly, should give rise to better quality crop products with a shorter development time (Figure 1B ). It was also envisaged that products would be created that otherwise would not be developed (Flavell 1992). Arabidopsis is not an ideal model for all features of plants but it is helpful for many features of most species. Other plants are being developed as models, in part to help compensate for the deficiencies of Arabidopsis and in part to provide additional support, or not, for hypotheses gained from Arabidopsis. These include rice for monocots, Medicago and Lotus for nitrogen fixing legumes, tomato for development, fruit biology and diseases and poplar as a representative for trees. In this paper, Arabidopsis is singled out because knowledge coming from it is so much further advanced overall and because of its major impact on plant science. Knowledge coming from other model species is omitted simply for convenience. Their complementary role, as models, to Arabidopsis for improving plants is beyond question. The explosion in knowledge on plants that has come about from studying Arabidopsis can be appreciated by simply noting the growth of publications on it. These come mainly from Europe, the USA, Canada, Australia and Japan. The success for plant science based on Arabidopsis raises a major dilemma. Is it time to shift funding away from the model(s) in order to fund transfer of the new knowledge to the crops on which society depends and will increasingly depend? The pressures, referred to above, are coming rapidly in parts of the world and it takes decades to produce and evaluate improved crops. I believe we are in danger of getting the strategy wrong, especially in failing to recognize and fund what is necessary to exploit the DNA-based information from models to improve crops. The absolute levels of funding are woefully inadequate, globally, and many new opportunities are going to waste. The ideal would be to sustain or expand the level of funding and intellectual appeal of the model species while also greatly expanding the development of the knowledge base to the crops. While the ideal might not be reached, the arguments for tackling the ideal to ensure a healthier planet are extraordinarily strong and very tangible. How will the balance/strategy be reached? There are, as always, many factors, scientific and non scientific, and I do not wish to elaborate them all here. However, it is appealing to consider what Arabidopsis and the other model plants have to offer crop science and what needs to be done to apply the knowledge to 369

6 crop improvement. The conclusion is that we cannot afford to drop investment in Arabidopsis and the other special models or not greatly increase the application of the knowledge gained from this and other models, if our objectives are world food sufficiency, renewable resources, sustainable management of the planet and world stability. Plant breeding The knowledge needed for efficient crop breeding is still substantial, even for those crops that have received the most R&D attention. Crop breeding as practiced to date is a time-consuming process being based on generating large numbers of gene combinations and evaluating the progeny in many locations and environments to find the plants that are superior and capable of improving the sustainability of farming, livelihoods and providing better industrial and consumer products. It has long been recognized that if it were known which genes (alleles) are available in existing accessions of a species and which gene (allele) combinations are required, then the breeding and selection processes could be speeded up and made more directed and less unpredictable. The development of methods to find and map easily assayed molecular markers for the species, covering all the chromosomal segments in fine detail, have provided the means of finding out on which chromosome segments the gene(s) are located which contribute to a particular trait (Paterson and Tanksley 1997; Xu 2002, 2003). This genetic mapping of so-called quantitative trait loci (QTLs) can provide a major boost to productivity in plant breeding when marker combinations are used to select plants carrying favorable alleles for traits difficult to measure. These genomics technologies need to be applied on sufficient scale but they are rarely used to manage many traits simultaneously because of cost, lack of vision, knowledge and commitment. Even when they are, this still leaves the problem of knowing the genes underlying the traits-the ultimate need for directed, efficient plant breeding. Until the genomes of crop species are at least roughly sequenced and the QTL mapping done to great resolution, the genetic basis of the QTLs will not be known. Even then the number of different genes and alleles contributing to a trait may be large and very costly to find without guidance from knowledge about gene-trait linkages gained from models or closely related crops. It is now becoming obvious that sequencing of plant genomes is valuable because it can reveal interspecies genetic synteny across small or very large chromosomal segments and this allows predictions of where QTLs are likely to reside once they have been determined in syntenic segments of another species (Gale and Devos 1998; Ku et al. 2000; Bennetzen and Ma 2003). This is a huge advance and is beginning to revolutionize crop genetics. Now the rice geneticist is helping the wheat, maize and sugar cane breeders for example, owing to the genetic synteny 370

7 between the grasses (Ahn and Tanksley 1993; Gale and Devos 1998). This synteny reflects the common evolutionary origin of species. The whole field of comparative genomics where discoveries of genes and traits in one species can be used to find and interpret genes and traits in another is very exciting and has been opened up by combining knowledge from both model and crop species. It illustrates the value and hence necessity of gaining complete, or near complete, DNA sequences for the chromosomes of all our crop species. That of rice is completed (Goff et al. 2002; Yu et al. 2002; International Rice sequencing Genome Project: and the genomes of tomato, Medicago, Lotus, poplar and corn are now well advanced (Bevan and Walsh 2004). The sequencing of wheat, barley and others are being planned. Once near-complete collections of gene sequences are available, from genomic or cdna sequencing, it allows the complements of genes, proteins and RNAs to be compared. The full length cdna sequences from Arabidopsis (Haas et al. 2002), corn ( and soybean ( have been very useful for interpreting the genomic sequences from all plant species, because of conservation of protein sequences during evolution. Most proteins in Arabidopsis have reasonably close counterparts in other species. (Ware and Stein 2003; Bevan and Walsh 2004; Rensink and Buell 2004). Promoters and regulatory sequences are not assessed in protein gene product analyses and these regulatory sequences are frequently the source of variation in species characteristics (Irish and Benfey 2004). Species-specific genes and species-specific variants can be easily recognized from such comparative genomics as well as all the genes in common. This is a launching point for leveraging the knowledge on one species to benefit another. It is also the launching point for DNA sequencing into different accessions of a species to discover the genetic variation around specific loci that is within the species. This, of course, can give rise to more chromosome segment markers for further QTL mapping and plant selection in breeding programs. It may turn out that there is no genetic variation for many genes in the species/population and then discovering the genes behind traits cannot be achieved by conventional genetics and, more importantly, it may not be possible to improve the traits using natural variation. In summary then, there remains the need to speed up the processes of plant breeding by being able to define traits in terms of known genes, to be able to identify the genes (alleles) rapidly and to bring more genetic variation into the species. For some species progress is substantial but this is a huge task when considered for all the species on which man depends. It will take a very long time to complete to a reasonably comprehensive extent at the present rate of progress. Full genome sequencing is essential to enable comparative genomics to be developed. A view of genomics-driven crop improvement is depicted in Figure 2. The information base referred to in the figure will contain chromosome sequences, genes sequences, gene expression data and gene-trait linkages from all species studied to 371

8 Figure 2. Crop development from a genomics-derived knowledge base. date and this information will guide selection of which breakthrough genes and gene combinations are required/hypothesized to create a better product. The genes can be alleles within the species or transgenes. The scheme is dependent on the efficient accessibility of all this information. This is far from simple as many of the relevant databases are not easily cross referenced and the gene nomenclature is currently far from uniform between species. This is being addressed however, especially by The Arabidopsis Information Resource (TAIR) in liaison with the other plant database (e.g. annotators (Berardin et al. 2004). The prototype development by breeding would have molecular assays at every step to ascertain that the right gene combinations are being selected. (Xu 2002, 2003) Of course, it is necessary to evaluate growing plants under agricultural conditions in multiple environments but finding the right plants to test should be quicker and fewer plants would need to be screened. The DNA-guided process is not cheaper but the additional cost should be offset by the faster rate of progress. Arabidopsis as a reference species What does Arabidopsis, (together with studies on other model species) and all the advances made via model species bring to plant breeding research? The most relevant contribution is the fast-growing information on gene-trait associations. Yet, its relevance to crop plants is in need of much more exploration a key emphasis of 372

9 this paper. Funding agencies and scientists in many countries have set goals to find out everything about a plant using Arabidopsis and make the information available to all in user-friendly forms. The Arabidopsis Information Resource (TAIR) in the USA is responsible for carrying out a functional annotation of every Arabidopsis gene using world-wide data and a controlled vocabulary, particularly that of the Gene Ontology system, in liaison with annotators of other plant genomes, to help transfer of information from Arabidopsis to other crops (Berardini et al. 2004). The National Science Foundation of the USA is funding the goal to describe the function of every plant gene by 2010, using all sorts of approaches (Somerville and Dangl 2000; Multinational Coordinated Arabidopsis Genomics Project 2003). The plant breeding community, therefore, can expect in the near future an extraordinary knowledge base to help improve plants in more directed ways. This is truly a revolution for plant breeding, especially when all the databases modeled after Arabidopsis and rice are added in. It could and should launch a new wave of plant breeding research on an unparalleled scale. Arabidopsis can be treated experimentally as if it were a crop and its features treated as crop traits. A compendium of such traits is given in Figure 3 for which Ceres has sought and found genetic variation, by mis-expressing plant genes under a strong promoter and measuring the traits in specially developed assays. These traits are those that any plant breeder would include in a list of assets to be Figure 3. Frequencies of modified phenotypes generated by mis-expression of single plant genes in Arabidopsis (unpublished results, Ceres, Inc.). 373

10 improved in many crops. Thousands of gene-trait associations have been established in Arabidopsis (TAIR), far more than is known for any crop species today. It is therefore now possible to predict an in planta function for thousands of crop genes from Arabidopsis studies. The important conclusion from current progress is that the rate of discovery of gene-trait linkages is so much higher for Arabidopsis than any crop, including rice, that not to explore the relevance of the Arabidopsis results more rapidly for crop plants is simply foolish. The costs of doing the equivalent primary work in crop species is so much greater and, crucially, so much slower. Not evaluating the relevance of Arabidopsis results more quickly is a huge opportunity cost for societies. This cost may be crucial in the decades to come. Results from the model are very relevant to crop biology as illustrated by the results on the developmental biology, biochemistry and physiology underpinning processes such as flowering control, tolerance to environmental stresses and diseases, etc. as discussed by Irish and Benfey (2004), Hayama and Coupland (2004), Griffiths et al. (2003) and Izawa et al. (2003). Thus the Arabidopsis results firstly provide hypotheses as to the function of orthologous genes in crops and secondly guide the breeder to which genes in the crop genome are likely to affect the trait in question. What are the information databases and resources that Arabidopsis brings to provide these cost-effective advantages? First, the collection of knock-out T-DNA insertions, established via transformation, that includes an insertion into most genes. Using these lines many gene-phenotype associations have been established but the phenotypes of many more of the plant mutant lines need to be assessed in many more environmental conditions and proof obtained that the phenotype is due to the defined gene insertion. Targeted searches for equivalent gene-trait associations can now be sought in crops focused on the orthologous crop genes. Knock-out lines reveal, of course, the effects of deleting the function of a gene or of inserting an additional piece of DNA in or adjacent to a gene. It can be argued that knockout effects are dissimilar from the natural variation underlying traits in breeding populations but knock-out lines are not expected to reveal the ideal mutation in a crop species. The point here is that the silencing mutation guides the crop breeder to a candidate gene(s) underlying the phenotype. Deleting a gene function sometimes does not produce any phenotype because there are other genes that duplicate the function. Although Arabidopsis has a small genome it still reflects its polyploid origin in having duplicated genomic segments. (Ku et al. 2000). It also has many multigene families. Nevertheless, it is probably likely that crops have more functional gene duplication and so Arabidopsis is a more suitable organism to find most of the gene-trait linkages. This is also the case because in Arabidopsis it is more readily possible to rapidly make double and triple mutants to uncover functions of duplicated genes. It is not likely that deletions of important genes will lead to improved phenotypes in Arabidopsis or crops, although this is true occasionally. However, this is not the point; it is knowledge of 374

11 gene-trait linkages that is important. Today, it is possible to use RNA interference to reduce expression of families of closely related genes which have very similar sequences. This approach enables gene expression to be reduced post-transcriptionally in a tissue-specific manner when the correct promoters are used to drive the RNAi constructs. Use of a model is very convenient for working out how to achieve such effects and the consequences of such post-transcriptional changes. The second relevant knowledge base is the growing collection of knock-in gene-trait associations that have been developed in the public domain and in companies such as Ceres ( Monsanto ( Icoria ( and Mendel ( in the USA. These plants are created by inserting genes from the same or another crop species, into Arabidopsis but under the control of a different promoter. The transgenes in these studies were created using the genomic sequence or full length cdnas (Haas et al. 2002). The transgenic lines are then screened for differences in many traits relevant to agriculture (Figure 2). Variant traits are then shown to be due to the transgene added. The genetic variation in these cases is due to the different levels of gene expression, either in the cells in which the genes are normally active or in the different cells in which the new promoter is active. It should be noted that these transgenes that determine modifications in traits act as single dominant genes. If these turn out to be useful in commerce they have the huge added advantage that they are easily assayed and tracked in a breeding program, directly and simply. Where the transgenes produce some benefit but also some deleterious effects, then changing promoters may optimize where and when the new gene is expressed. This is another area where Arabidopsis, together with its portfolio of promoters, can be used to test ideas about optimizing traits before spending a major resource on doing early experiments in crops. The gene-trait association knowledge from knock-in mutants can also direct attention to candidate genes in QTL mapping to find and exploit sources of natural variation in breeding programs, as described above for knock-out mutants. This may emerge as very useful for many crops. In addition, the information promotes hypotheses as to which transgenes should be inserted into crops to create specific, novel, valuable genotypes. Genes work through complex control networks, transcriptional and post-transcriptional. Their protein and or RNA products are similarly organized in time and space to function in networks. Metabolites also work in networks. This complexity is bewildering and it will take a huge effort to understand the mechanisms and systems behind gene-trait linkages. Here the use of a model is even more essential. One of the early ways in which this complexity is being tackled is to explore how genes are expressed in each organ/tissue under various environmental conditions. It is then possible to group genes into different sets and explore the functional linkages between each member of the set. By combining the knowledge of the knock-out and knock-in results with expression data, diagrams and computer simulations of 375

12 the networks are being formulated. From these, hypotheses are formulated and then can be readily tested in Arabidopsis much faster than in crops. Huge numbers of experiments have already been carried out on Arabidopsis addressing how all its genes are regulated during development and in many different environments. All these are being collated via TAIR and this provides a very rich source of information from which to understand the genetic basis of traits. Similar databases are being built up of metabolites. As the questions being asked about crop traits are often more complex then the use of a model is even more essential and cost effective to answer them. The real basis of traits will only be understood and managed well genetically when the systems biology of the trait under various conditions and knowledge of which steps are rate-limiting and under which circumstances are known in a range of species variants. For this, the need for initial research on model plants to focus the hypotheses to be addressed in crops seems inescapable. Testing of hypotheses from models in crops All the points made above for the use of models to discover the basic systems biology of traits and then testing the hypotheses in crops seem obvious. Yet, given the urgency to improve the efficiency of plant breeding and to remove the constraints how will the rapidly growing information from the models get evaluated and transferred to the key crops? Who will fund it? Who will do it? In the USA and Europe where there has been a decline in plant breeding in the public sector and much of breeding is now in the private sector, the issue appears to be falling between the two sectors. There has been a decline in people trained to be familiar with the germplasm on which successful plant breeding must be based and declines in facilities in the public sector to carry out field trials. The needed research is too preliminary and expensive for the private sector, with the exception of the most economically successful, and so they are unlikely to test most of the hypotheses. This is a serious situation where no sector is well-placed to solve the problem and provide a solution in a sustained way for decade after decade. It clearly is the public sector, in collaboration with the private sector in some instances that must do it. In Asia and South America, plant breeding is still based mostly in the public sector but resources have been relatively inadequate in the past. New funding and training strategies are thus needed to test in crops, on an adequate scale, the hypotheses coming from Arabidopsis and other model plants. The need is urgent. People need to be trained. Careers in this topic need to be made more attractive. The future quality of life for all will probably depend on it. Governments and scientists should not shirk the responsibilities. The genomics knowledge base on the models is growing wonderfully. It must be put to use for mankind as rapidly and purposefully as possible. The regulations and costs asso- 376

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14 Xu Y (2002) Global view of QTL: rice as a model. In: Kang MS (eds) Quantitative genetics, genomics and plant breeding. CAB International, Wallingford, UK pp Xu Y (2003) Developing marker assisted selection for breeding hybrid rice. Plant Breed Rev 23: Yu J, Hu SN, Wang J, et al (2002) A draft sequence of the rice genome (Oryza sativa L.ssp. indica) Science 296:79-92 Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135: Acknowledgements I am grateful to all my colleagues in Ceres, Inc. for continuing to formulate the ideas in this chapter and for the unpublished results referred to in the figures. 378