Focus on Roots

It is common for plant biologists to point out the importance of the neglected, hidden segment of plants that are their roots. It is striking to contemplate how much a better understanding of roots could contribute to the challenges facing agriculture today, namely a better use of fertilizer and water, as well as sustained productivity under various abiotic and biotic stress conditions. Yet, going through the pages of this Focus Issue dedicated entirely to roots, one becomes acutely aware of the formidable challenges that researchers are facing when tackling this plant organ, and one is reminded of all the good reasons not to work on this part of the plant. The nature of roots is to bury themselves into the soil and to enter into most intimate contact with their substrate, such that it is very hard to observe their growth and development, much less to extract them from the soil intact. Moreover, the soil is a substrate of mind-boggling heterogeneity and complexity, its complicated chemical and physical structure being potentiated by the biological diversity in the form of microbial communities. Luckily, an understanding of the fundamental mechanisms underlying root growth and development can be obtained in the beautifully simple, controlled, and protected system of agar-grown, young Arabidopsis (Arabidopsis thaliana) plants. Although highly artificial, this system has proven extremely amenable to analysis, and the Arabidopsis root meristem is arguably better studied and understood than most aerial plant organs, providing an invaluable basis for colleagues taking up the challenge of working on root systems of crop plants under more natural conditions. The Roots Focus Issue is a great illustration of this creative arc in current root research, spanning from work on model experimental systems such as Arabidopsis, to crops, and even to trees.

In the drive from Arabidopsis to other plants systems, it is often forgotten that the power of Arabidopsis has less to do with the availability of genome sequences and the ability to easily interrogate transcriptomes, things that are now available in many organisms, and more to do with the ease by which gene functions can be determined through knockouts and genetic transformations. In addition, Arabidopsis remains unrivaled in its ability to be imaged by confocal microscopy, a consequence of its very thin and low-fluorescent root system. In this Focus Issue, Ron et al. (2014) present a set of inspiring tools for the tomato (Solanum spp.) hairy root system, demonstrating how cell type-specific transcriptome profiling, confocal imaging of fluorescent reporters, and the latest cluster regularly interspaced short palindromic repeats technology can be combined into a powerful system for investigating root biology outside Arabidopsis.

The articles of Bucksch et al. (2014) and Zarebanadkouki et al. (2014) tackle the problem of root imaging. Bucksch et al. (2014) present a system for imaging and analysis of complex, soil-grown root systems of monocot and dicot plants. Zarebanadkouki et al. (2014) used neutron radiography of deuterium-labeled water to follow its radial and axial path through the root.

If this Focus Issue is a good reflection of the current trends in root biology, then clearly two topics are in the forefront of our colleagues’ minds: the study of root system architecture and the investigation of roots with their associated microbiome.

The simple, iterative structure of the root can give rise to an impressive complexity of different root system architectures, by playing with growth rates and direction of primary and secondary roots and adapting initiation rate and angles of lateral roots. Two articles in this Focus Issue address fundamental aspects of root meristem function. Kumpf et al. (2014) investigated how coordination of cell division between daughters of root meristem initials and their shift into endo-reduplication and elongation is important for correct root meristem function. Wang et al. (2014) studied the establishment and regeneration of the rice root cap.

Possibly all known plant hormones have been demonstrated to affect some aspect of root growth traits, and it is their complex interactions that determine the overall root system architecture. The article by Maloney et al. (2014) reports on the effect of flavonols on auxin transport and lateral root formation. The articles by Saengwilai et al. (2014) and Postma et al. (2014) highlight how root system architecture can influence the capacity of roots toward efficient nitrate uptake and how different architectures are optimal for uptake of distinct nutrients. Hufnagel et al. (2014) investigated how Sorghum bicolor homologs of PSTOL are associated with root system architecture and nutrient acquisition. Not only does root system architecture influence the uptake of nutrients, but nutrient availability has a major influence on the root system, leading to an intriguing regulatory cycle. Singh et al. (2014) demonstrate how phosphorous starvation influences the brassinosteroid signaling pathway, thereby affecting root architecture, providing an important example of how nutrients and hormones interact to adapt root development.

The importance of root system architecture is also reflected in the Updates of this Focus Issue, four of which discuss different aspects of root architecture regulation. Atkinson et al. (2014) review the developmental mechanisms behind root architecture traits and provide a comparison across species. Giehl and von Wirén (2014) discuss our current knowledge of how roots adapt their development for more efficient nutrient foraging. Evolution has tinkered with root system architecture in manifold ways, and Ristova and Busch (2014) provide an overview of how natural variation of root traits can be harnessed, not only for improvement of root traits but as a way to identify unique players in root development that were missed by genetic screens in the standard Arabidopsis genotypes. Kapulnik and Koltai (2014) introduce the less known hormone strigolactone and review its role in controlling root system architecture and also its involvement in nutrient foraging through cross talk with auxin.

Intriguingly, strigolactone is also released by roots in response to low phosphate’s providing a signaling bridge between root nutrient foraging and the soil microbiome. This signaling allows the development of mycorrhizal and rhizobial symbioses and is also hijacked by parasitic plants during host recognition. The rhizosphere microbial community and the composition of both plant and microbial secretions in this interface between root and soil are reviewed by Lakshmanan et al. (2014) and De-la-Peña and Loyola-Vargas (2014). Both reviews highlight the critical, yet poorly understood, nature of the complex root soil interface for plant health and its future potential to enhance agricultural productivity.

To remind us that it is not only root architecture that responds during nutrient foraging, Zelazny and Vert (2014) present an Update detailing how roots also internally reorganize at the cellular and molecular level during their search for nutrients. By modulating both the amount and the location of ion transporters, roots are able to drive efficient uptake, radial transport, and translocation to the shoot, matching nutrient supply with demand. This exquisite capacity of roots to supply nutrients and water to the developing plant requires balancing the modulation of both the macroscopic architecture of the root and the cellular and subcellular distribution of transporter in the root. Such a balancing act has driven the evolution of a strange feature of roots: its inner barrier, the endodermis. Two reviews address the importance of this barrier as a signal integration hub and a selectivity filter (epithelium) to nutrient and water transport. It was the evolution of roots driven by selection for resource acquisition from proto soils that allowed plants to colonize the land. Kenrick and Strullu-Derrien (2014) provide a fascinating glimpse into this process by reviewing what the fossil record tells us. Kenrick and Strullu-Derrien (2014) close with a discussion of how, amazingly, the evolution of roots has affected the Earth’s geochemical cycle. This is a fitting reminder of the critical importance of plant roots, an organ that can easily be overlooked as it buries itself out of sight into the soil.