Opinion The roots of a new green revolution Griet Den Herder1,4, Gert Van Isterdael2,3, Tom Beeckman2,3 and Ive De Smet2,3 1 Genetics, Faculty of Biology, University of Munich (LMU), D-82152 Martinsried-Mu¨ nchen, Germany 2 Department of Plant Systems Biology, VIB, Technologiepark 927, 9052 Gent, Belgium 3 Department of Plant Biotechnology and Genetics, Ghent University, Gent, Belgium 4 Current address: Ablynx nv, Technologiepark 21, 9052 Gent, Belgium A significant increase in shoot biomass and seed yield food production has often been overlooked. Nevertheless, has always been the dream of plant biologists who wish the root system is taking care of indispensable plant func- to dedicate their fundamental research to the benefit of tions such as uptake of nutrients and water, anchorage in mankind; the first green revolution about half a century the substrate and interaction with symbiotic organisms. ago represented a crucial step towards contemporary Consequently, root system development is central for the agriculture and the development of high-yield varieties plant to reach optimal growth and is sure to contribute to of cereal grains. Although there has been a steady rise in the levels of yield obtained in crops. Lately the impact of our food production from then onwards, the currently the ‘hidden half’ on plant growth has become apparent not applied technology and the available crop plants will not only in Arabidopsis (Arabidopsis thaliana), but also in be sufficient to feed the rapidly growing world popula- crops like wheat (Triticum aestivum), rice (Oryza sativa), tion. In this opinion article, we highlight several below- maize (Zea mays) and legumes, such as soybean (Glycine ground characteristics of plants such as root architec- max), barrel medic (Medicago truncatula), and Lotus japo- ture, nutrient uptake and nitrogen fixation as promising nicus [6–12]. Moreover, recent simulations suggested that features enabling a very much needed new green revo- changes in root architecture can strongly affect yield, lution. which might be sufficient to explain maize yield trends in the USA Corn Belt [13]. This indicates that root growth Rise of the hidden half and development might represent an underestimated and In 1798 Thomas Robert Malthus predicted in his An Essay not fully exploited area for strategies to enhance yield. on the Principle of Population that sooner or later a con- tinuously growing world population will be confronted with What are the major challenges? famine, disease and widespread mortality [1]. About two Due to climate change, plant roots and their habitats have hundred years later, the world is facing the major chal- a high risk of becoming subjected to unfavorable conditions lenge of providing food security for an ever growing world such as water scarceness, increasing ground water salini- population, while the agricultural area is shrinking [2].In ty, decline in soil nutrients and build up of soil pests. In the middle of the previous century, a Green Revolution addition the available arable land is becoming more sparse allowed food production to keep pace with worldwide pop- and precious due to erosion of hill-sides, soil degradation, ulation growth [3]. The International Food Policy Research landslides and the increasing demand for biofuels. The Institute has launched the 2020 Vision Initiative with the contemporary yields obtained by the classical use of water, primary goal to reach sustainable food security for all by fertilizers and pesticides have reached a maximum. 2020 and to cut by 50% the number of chronically under- Attempts to further boost yield by using more fertilizers nourished people on the planet by the year 2015 (http:// and/or pesticides are not feasible, not only because of a www.ifpri.org/book-753/ourwork/program/2020-vision- higher risk for public health and environmental problems, food-agriculture-and-environment). These deadlines are but also because of negative effects on yield [14]. For the approaching quickly, and we are far from reaching either root system to live up to the expectations as an important of these goals. In the immediate future, plant research will contributor to improved yield, a number of challenges will again be central in finding alternative crops or methods to need to be tackled (see also Box 1). cope with the threatening food shortage. In addition, next First, the conversion of unsuitable soil to arable land to finding the ideal food–population balance, improving will require agricultural techniques such as the improve- plant yield will also be vital for exploiting plants further ment of soil conditions through alternative fertilization. as a renewable energy source. Unfortunately, plant growth For instance, legume crop rotations as green manure have and productivity are greatly affected by environmental contributed considerably to the improvement of soil quality stresses such as drought, high salinity, nutrient-deficiency [15]. Second, and more critical, those soils will require and adverse temperatures. Due to climate changes these crops which are able to deal with the awkward edaphic challenges are currently becoming even more intensified. and climate conditions. We will need to improve root In the past, improvement of crops and agricultural architecture, nutrient uptake efficiency, nutrient storage techniques has mainly focused on increasing shoot biomass and root-to-shoot transport. Furthermore, roots need to and seed yield [4,5], and the relevance of the root system for fight off pathogens, prevent loss of soil through erosion and be able to resist the increasingly occurring unfavorable Corresponding author: De Smet, I. ([email protected]). conditions such as salt and drought. The past decade 600 1360-1385/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2010.08.009 Trends in Plant Science, November 2010, Vol. 15, No. 11 Opinion Trends in Plant Science Vol.15 No.11 Box 1. Hardest questions and a roadmap for root biology Box 2. The value of root research in the model plant Arabidopsis To obtain the necessary adaptations to root system architecture and symbiotic interactions, a couple of hurdles need to be taken first. A major challenge of studying model organisms, such as Arabi- How to translate the knowledge from conditioned, agar-grown dopsis, is transferring the knowledge and new tools to crop species model plants to soil-grown roots? How to translate the knowledge [4]. However, investigating root development in Arabidopsis has the from a simple Arabidopsis or legume model root system to a advantage that crucial genes can be more easily identified using complex crop? Next to answering these questions, as attempted genome-wide tools and integrated approaches, and quickly tested, throughout the main text, a number of key things that are needed upon which their function can be analyzed in crop species. For are: example, through a focused, cell-specific transcript profiling of early A better understanding of root development and its interaction lateral root initiation we recently identified a ligand-receptor-like with the biotic and abiotic factors, as well as with the symbiotic kinase pathway centered around ACR4 that controls aspects of root organisms in the rhizosphere. branching in Arabidopsis [93]; and it will be interesting to analyze More detailed analyses of the impact of root development on the role in root development of the maize ortholog CR4, the plant fitness, and consequently on the communication between founding member of this subset of receptor-like kinases [94]. root and shoot. However, because cereals display a more complex root branching Integration of all aspects of root biology in the simple models that than Arabidopsis [8] it is clear that direct studies in maize, rice, exist for root meristem functioning and branching [87–91], and to barley (Hordeum vulgare subsp. vulgare L.), or the new cereal create models that implement the influence of root environmental model purple false brome (Brachypodium distachyon) play an conditions, such as nutritional sources and soil organism equally important role [95–98]. These and other species already associations [92]. revealed key regulators of (lateral) root development, before they were described in Arabidopsis [96,99–101]. In addition, Arabidopsis does not engage any root symbiosis, and therefore, these aspects provided an enormous leap forward with respect to our need to be addressed in model legume systems. Furthermore, more understanding of the physiological and molecular aspects research opportunities directly in the species of interest are arising, due to the increasing amount of knowledge and availability of of root development and branching in Arabidopsis [16] and genomic tools in crops, as well as the new sequencing technologies crops like maize and rice [6,8], as well as of root interac- which allow us to (re)sequence whole genomes and identify trait tions with pathogenic or beneficial organisms [17–19]. mutations in a straightforward manner in the crops itself. Never- Nevertheless, we are only at the verge of understanding theless, Arabidopsis will remain an excellent model system to study this complex process in its entirety. The remaining gaps in the basic elements of root architecture and adaptation to the environment, because of the vast knowledge on the developmental, our knowledge impede a speedy translation to agricultural physiological, and genomic level, and simplicity of the root system. applications and need to be filled by well thought-through