New insights to lateral rooting: Differential responses to heterogeneous nitrogen availability among maize root types

Abstract

Historical domestication and the "Green revolution" have both contributed to the evolution of modern, high-performance crops. Together with increased irrigation and application of chemical fertilizers, these efforts have generated sufficient food for the growing global population. Root architecture, and in particular root branching, plays an important role in the acquisition of water and nutrients, plant performance, and crop yield. Better understanding of root growth and responses to the belowground environment could contribute to overcoming the challenges faced by agriculture today. Manipulating the abilities of crop root systems to explore and exploit the soil environment could enable plants to make the most of soil resources, increase stress tolerance and improve grain yields, while simultaneously reducing environmental degradation. In this article it is noted that the control of root branching, and the responses of root architecture to nitrate availability, differ between root types and between plant species. Since the control of root branching depends upon both plant species and root type, further work is urgently required to determine the appropriate genes to manipulate to improve resource acquisition by specific crops.

Abbreviations

LR

lateral root

LBD

LATERAL ORGAN BOUNDARIES-DOMAIN

PIN

PIN-FORMED

Recent Insights to the Control of Root Branching – Differences Between Root Types

Domesticated monocotyledonous-crops, such as maize, wheat and rice, show more complex root system architectures than the traditional, dicotyledonous, model plant, Arabidopsis thaliana.^1,2 In all species, however, the branching of lateral roots improves belowground resource capture by increasing root surface area and contact with the soil solution.^3-6 The extent of root branching is influenced by both the local availability of soil resources and the demand of the plant for these resources, which is often reflected in the tissue concentrations and fluxes of specific hormones.^7,8 Several recent reviews have provided a comprehensive description of the genetic, genomic and cellular processes involved in root branching in various model plants.^9-12 Despite this progress, much detail remains to be clarified and confirmed in crop species, especially in relation to root responses to heterogeneous nutrient availability. For example, maize shows contrasting responses of lateral roots to local nitrate concentration during development.^13,14 The induction of lateral root (LR) elongation by heterogeneously distributed nitrate is relatively similar in both embryonic and post-embryonic roots, but this is not true for the induction of LR initiation.^13-16 A deeper knowledge, and understanding, of the contrasting responses of different root types to exogenous and endogenous signals initiating root branching are needed.

The Initiation of Lateral Roots–Differences Between Plant Species

A “steep, cheap and deep” ideotype has been proposed for a maize root system optimized for water and nutrient acquisition.¹⁷ Many studies indicate an active role of LRs in capturing soil resources and increasing yields of maize.⁴ In A. thaliana, LRs are initiated from pericycle cells.¹⁸ Before initiation of LRs, pericycle cells have to be re-activated from the stem-pericycle cell group, which is effected by both endogenous and external signals.^19-21 Although cereals may share a common pathway controlling LR initiation via the division of pericycle and endodermis cells with A. thaliana,^1,24 the formation of LRs in cereals is primarily regulated by alternative root-type-specific pathways.^22,23 However, knowledge of LR initiation in cereals is largely derived from studies of mutants, and all mutants exhibiting LR phenotypes show these only in embryonic roots.^25,26 It has, therefore, been suggested that the regulation of root branching in cereals must differ between embryonic and post-embryonic roots.^10,27 Closely related monocot and dicot LATERAL ORGAN BOUNDARIES-DOMAIN (LBD) proteins probably act early in auxin signaling in the root system, yet in different developmental contexts.²⁸ LBD proteins in maize and rice are involved in shoot-borne root formation while their closest homologs in A. thaliana regulate LR initiation.²⁸ The LBD phylogeny shows distinct evolution of molecular mechanisms for root initiation downstream of auxin in lycophyte and euphyllophyte roots.²⁹ A more detailed comparison of the distinctive aspects of LR formation, and the development of shoot-borne roots, in different plant species might address how evolution, or domestication, has influenced their different responses in root branching to the environment.

Monocot-Specific Auxin Transport and Redistribution Triggered by Nitrate

Auxin affects a wide range of developmental processes. It appears to be part of long-distance N-signaling to adjust root growth in systemic and local responses to nutrients availability both in A. thaliana and maize.^15,30-34 Biosynthesis and catabolism, intercellular and intracellular transport of auxin and its role in plant development have been reviewed in detail.³⁵ Auxin transport contributes crucially to the generation of local auxin maxima, which guide the given cells to switch their developmental program. The asymmetrical distribution of plasma membrane-localized, PIN-FORMED (PIN) transporters determines the directionality of auxin flow. Phylogenetic and gene structure analyses, together with the expression pattern of the maize PIN gene family, indicate that sub-functionalization of some ZmPINs are associated with the differentiation and development of monocot-specific organs and tissues.³⁶ Monocot-root specific PIN9 has been identified in maize, rice and wheat.^36-38 Higher expression of OsPIN9 is found in the root and stem-base compared to other tissues in rice.³⁸ ZmPIN9 is exclusively expressed in nodes and roots in maize.^36,38 In the region where LRs develop, monocot-specific PIN9 was highly expressed in the LR primordia, pericycle cells and vascular tissue in rice, and in the endodermis, pericycle, and phloem of central cylind er of maize.^36,38 Monocot-specific developmental process of LR formation may be related to unique auxin flows determined by the distinctive PINs found in such plants.

Ideal Root Traits: Domestication-Reflected Plastic Responses

Improvement of maize to overcome environmental stresses, rather than for primary productivity has been the main driver for obtaining higher grain yields in new maize hybrids.³⁹ Strategies to improve N fertilizer use efficiency include using genetic modification and breeding new hybrids, which acquire more N from soil and utilize the acquired N more efficiently.^40,41 In modern breeding environments, root traits display a high degree of adaptation to the high nutrient inputs that are present during selection.⁴² In the future, selection for root traits, and root architectural ideotypes, that optimise resource capture with reduced inputs are advocated.^17,43,44 Traits related to root lodging resistance, improved root function, enhanced nutrient capture, and increased resource interception have all been explored in recent years.^17,45-47 Target genes for the manipulation of root architectural traits have been extensively cataloged.^44,48 In addition, the highly flexible responses in root branching to the heterogeneous distribution of soil resources might be exploited to improve root foraging capabilities. Root responses of maize hybrids to abiotic stresses are often more dramatic than those of inbred lines,^49,50 and lateral branching in response to heterogeneous nitrate distribution is no exception (Yu et al., unpublished). However, since the control of root branching depends upon both plant species and root type, further work is urgently required to determine the appropriate genes to manipulate in this context to improve resource acquisition by specific crops.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Funding

We thank the National Natural Science Foundation of China (No. 31272232), the State Key Basic Research and Development Plan of China (No. 2013CB127402), Chinese Universities Scientific Fund (No. 2012YJ039), the Post-graduate Study Abroad Program of China Scholarship Council and the Rural and Environment Science and Analytical Services Division (RESAS) of the Scottish Government for financial support.