Rooting for survival: how plants tackle a challenging environment through a diversity of root forms and functions

Abstract

The current climate crisis has global impacts and will affect the physiology of plants across every continent. Ensuring resilience of our agricultural and natural ecosystems to the environmental stresses imposed by climate change will require molecular insight into the adaptations employed by a diverse array of plants. However, most current studies continue to focus on a limited set of model species or crops. Root systems are particularly understudied even though their functions in water and nutrient uptake are likely pivotal for plant stress resilience and sustainable agriculture. In this review, we highlight anatomical adaptations in roots that enable plant survival in different ecological niches. We then present the current state of knowledge for the molecular underpinnings of these adaptations. Finally, we identify areas where future research using a biodiversity approach can fill knowledge gaps necessary for the development of climate-resilient crops of the future.

Figure 1.

Root system architecture and anatomical responses to different habitats. A) Desert environment. A date palm tree on the left and cactus plant on the right. Date palms have secondary root structures called pneumatophores that form near the soil surface. A cross-section diagram of a date palm root showing a suberized epidermis, exodermis, endodermis, and fiber cells. Aerenchyma tissues surrounding the central vasculature (bottom, left). A representation of a determinate meristem that form in some cacti species, with root hairs along the epidermis layer. Figure modified from (Kirschner et al. 2023). B) Aquatic environments. A water lily root cross section with a lignified epidermis, endodermis, and astrosclereids. The hypodermis contains suberin. Aerenchyma tissue surrounding the central stele. C) Mangrove ecosystem. Common root structures of mangroves species including prop/stilt (left), buttress (middle), and pneumatophores (right). Root cross section diagrams of prop/stilt roots (bottom, left) and pneumatophores (bottom, right), highlighting differences in anatomical structures. D) Nutrient-deficient environments. White lupin plant with rootlets stemming from the pericycle of a cluster root. The panel to the right shows the anatomical structures involved in rootlet formation and differentiation. E) Plant host environments. 1. Parasitic plants form terminal haustoria (upper left) and lateral haustoria (upper right). An illustration of striga contacting a host root and forming haustorial hairs from the root apical meristem. Haustorial hairs penetrate the host until they reach and make connections with the vasculature of the host. Lateral haustoria differentiation of several root layers. The outermost layer also forms root hairs to secure attachment and invasion of the host. 2. Epiphytic plants attach to a host but do not invade. Some can form specialized photosynthetic roots with a spongy velamen radicum layer, allowing for absorption of moisture and nutrients from the air.

Figure 2.

Genetic pathways controlling root hair plasticity. A) Genes involved in patterning of the root epidermis identified through studies in A. thaliana. In atrichoblast cells, a protein complex consisting of WER, TTG1, and GL3/EGL3 activates the transcription factor GL2 to repress root hair formation. The absence of WER in trichoblast cells results in a protein complex that is unable to activate GL2 to allow root hair development. The patterning of the root epidermis is also influenced by non-cell autonomous functions of JKD (from the cortex) and WRKY75 (from the stele). B)A. thaliana roots exposed to extended periods of phosphate deficient conditions show increased cortical cell divisions. This in turn influences the number of trichoblast cells in the epidermal cell layer, resulting in an increase in root hair number in phosphate-deprived conditions (Janes et al. 2018). C) Adaptation to short-term phosphate and nitrate deficiency results in increased root hair length and density, while iron deficiency causes branched root hairs (Müller and Schmidt 2004). These changes increase the root surface area available for nutrient absorption. D) Auxin and cytokinin signaling pathways influence root hair development under phosphate- and nitrate-deficient conditions. Auxin regulates root hair development through ARF19 in low-phosphate conditions, while changes under low-nitrate conditions depend on ARF6/8. The ubiquitin ligase UBIQUITIN-CONJUGATING ENZYME controls branching of root hairs observed under iron-deficient conditions.

Figure 3.

Pathways involved in patterning and differentiation of the ground tissue. A) In A. thaliana primary roots, a target of the SHR-SCR protein complex, CYCD6;1, controls division of the cortex-endodermal initial cell, resulting in the 2 cell files of the ground tissue (cortex and endodermis). In older roots, periclinal divisions in the endodermal cell file form an extra ground tissue layer usually referred to as the middle cortex. The formation of the middle cortex is regulated by the hormones ethylene, gibberellic acid (GA), and abscisic acid (ABA) as well as reactive oxygen species (ROS). In another Brassicaceae species, C. hirsuta, the middle cortex development occurs earlier in development and is regulated by the transcription factor PHB. The expression of miR165/166 was found to be lower in the endodermis of this species compared with A. thaliana, allowing the expansion in expression domain of its target, PHB. B) A differentiated endodermis in A. thaliana roots consists of 2 barriers for solute transport, the lignin-rich Casparian strip and suberin lamellae (left). S. lycopersium and S. tuberosum roots also contain a similar endodermal layer (middle). In addition to this, these species also contain an outer exodermal layer that displays a characteristic polar lignin cap and suberin lamellae. In O. sativa, the exodermis contains Casparian strip and suberin lamellae similar to the endodermis (right). C) Ethylene levels increase in maize roots experiencing hypoxic conditions caused by water-logging. This elevated ethylene triggers cell death leading to the formation of aerenchyma. The transcription factor, bHLH121, promotes the development of aerenchyma in maize roots. D) Hypoxic conditions also trigger aerenchyma formation in the rice and wheat roots as well as in A. thaliana hypocotyls, with auxin and salicylic acid playing key roles in this process.

Figure 4.

Genetic regulators of parasitic plant-host interactions. The successful invasion of the host by a parasitic plant involves loosening of the cell wall by β-1,4 glucanases and perception of the host-derived ethylene by the parasite. The differentiation and establishment of vascular connections in the haustoria is dependent on cytokinin and ABA signaling.