Abstract
Background
The rhizosphere is the interface between roots and the soil and the site of nutrient and water uptake for plant growth. Root anatomy and the physical, chemical, and biological components of the rhizosphere interact to influence plant growth. Several root developmental and rhizosphere signals combine in the patterning of root cortical anatomy and have implications for the plant’s hydro-mineral nutrition and carbon partitioning and therefore crop productivity, especially in edaphic stress.
Scope
Here, we highlight how mutualistic mycorrhizal fungi from the rhizosphere mobilize plant molecular actors controlling root anatomical traits, including cortical cell size, to facilitate their establishment and accommodation within the cortex. We explore the effects on plant growth and stress tolerance that may result from the changes in root anatomy driven by interactions with arbuscular mycorrhizal fungi, including altering the metabolic efficiency required for nutrient exploitation. We also discuss opportunities for understanding the genetic control of root anatomy and rhizosphere interactions to enable a comprehensive understanding of the benefits and trade-offs of root-rhizosphere interactions for more productive crops.
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Introduction
In the next 25 years, food production needs to be doubled to meet the demands of the growing population (Hunter et al. 2017). This challenge is further complicated by climate change, where altered weather patterns, increasing temperature, degrading soil quality, and depletion of freshwater resources will reduce the regions and growing seasons suited for agricultural production (IPCC 2021). Thus, we urgently need novel strategies to develop crops with improved resource efficiency. Roots play a critical role in the efficiency of soil resource acquisition and dynamically interact with the soil matrix around the root (defined as the rhizosphere) to influence stress adaptation and yield. One promising approach for the development of crops with improved resource efficiency is selecting varieties with root anatomical traits that enhance interactions with beneficial microorganisms from the rhizosphere, with positive effects on plant hydro-mineral nutrition and abiotic stress tolerance (Galindo-Castañeda et al. 2022).
Root anatomy differs substantially both within and among species (Enstone et al. 2003; Lynch et al. 2021). Optimization of root anatomical traits such as root cortical cell size, root cortical cell wall thickness, root cortical cell file number, or root cortical aerenchyma can reduce the nutrient and respiratory demands of root tissues, enabling greater acquisition of soil resources for a given level of metabolic investment and improving yield under stress (reviewed in Lynch et al. 2021). In addition, anatomical traits can influence root oxygen availability (Kotula et al. 2009), and exudation of chemical signals (Canarini et al. 2019), impacting root associations with microorganisms in the rhizosphere (as reviewed in Lynch et al. 2021; Galindo-Castañeda et al. 2022).
Root and rhizosphere interactions can be beneficial, neutral, or antagonistic in terms of plant fitness. Root associations with arbuscular mycorrhizal fungi are one such example of potential positive interplay between the root and rhizosphere. The arbuscular mycorrhizal fungi develop an extensive network of hyphae that grow both in the rhizosphere and intercellularly in the root cortex, thereby functionally extending the root system. In the root, hyphae grow into individual cortical cells where they develop highly branched hyphal structures, arbuscules, where inorganic nitrogen, phosphorus, and other minerals are unloaded for plant growth in exchange for photosynthetically derived lipids and carbohydrates. Arbuscular mycorrhizal symbiosis can provide up to 40% nitrogen and 80% phosphorus uptake in rice and increase yield by 30% in maize (Yang et al. 2012; Ramírez-Flores et al. 2020; Wang et al. 2021).
There has been significant progress in understanding the signaling associated with the early stages of arbuscular mycorrhizal symbiosis (e.g., Kosuta et al. 2003; Besserer et al. 2006; Choi et al. 2018). Root infection by the fungus and development of arbuscules necessitate a substantial transcriptional reprogramming process, involving the exchange and perception of signals between the plant and fungus (Lanfranco et al. 2018). This reprogramming is orchestrated by plant transcription factors that play a crucial role in effecting root morphological and developmental changes essential for the accommodation of arbuscules (Gobbato et al. 2012; Wang et al. 2012; Volpe et al. 2013; Foo et al. 2013; Devers et al. 2013; Xue et al. 2015; Park et al. 2015; Heck et al. 2016; Floss et al. 2017; Russo et al. 2019; Choi et al. 2020; Seemann et al. 2022). Interestingly, there is evidence that rhizosphere signals from arbuscular mycorrhizal fungi influence root cortical patterning (Heck et al. 2016; Seemann et al. 2022). A better understanding of the interplay of rhizosphere and plant signals is directly relevant for improving plant hydro-mineral nutrition, and therefore plant growth and abiotic stress tolerance.
How may the interplay of mycorrhizal fungi arbuscule development and genetic control of root cortical traits be exploited for crop improvement?
Root growth depends on mechanisms balancing cellular axial and radial expansion in the elongation zone. Root cell axial expansion has been associated with gibberellin/DELLA signaling in Arabidopsis (Ubeda-Tomás et al. 2008). It was shown that the gibberellin-mediated destabilization of DELLA proteins of the GRAS family in the endodermis promoted anisotropic growth in the cortex (i.e., axial expansion) while disruption of this gibberellin response by expressing a stabilized DELLA protein slowed anisotropic cell growth causing radial expansion of cortical cells. SCARECROW-LIKE 3 (SCL3), another GRAS transcription factor, acts as a positive regulator of the gibberellin pathway and DELLA repressor, and works in conjunction with the SHORTROOT–SCARECROW (SHR-SCR) stem cell program to coordinate ground tissue elongation during root development (Zhang et al. 2011).
DELLA proteins also play essential roles in regulating the establishment of arbuscular mycorrhizal symbiosis. They are important in the initial stages of arbuscule development when the host cells increase their size to accommodate the fungal structure. In Medicago, MYCORRHIZA INDUCED GRAS1 (MIG1) is induced in cortical cells colonized by the fungus and interacts with DELLA to promote radial cell expansion and allow arbuscule development (Heck et al. 2016). Recently, MYCORRHIZA INDUCED GRAS2 (MIG2) was identified as another positive regulator of radial cortical cell expansion during arbuscule formation in Medicago roots (Seemann et al. 2022). Conversely, MYCORRHIZA INDUCED GRAS3 (MIG3) restrains cortical cell growth and is a negative regulator of arbuscule development (Seemann et al. 2022). Overexpression of MIG1 and MIG2 increased cortical cell size, cortical cell file layers and root diameter (Fig. 1) while overexpression of MIG3 has opposite effects on cortical cell size and root diameter in the absence of mycorrhizal fungus (Seemann et al. 2022). In the presence of mycorrhizal fungus, overexpression of MIG1 and MIG2 have no impact on root fungus infection and arbuscule development (Seemann et al. 2022).
MIG1 and MIG2, and their homologues in crop species, represent opportunities for enhanced stress adaptation through both enhanced accommodation of the fungal structure and the genetic manipulation of root cortical cell size which may have additive or even synergistic effects on plant drought and nutrient stress tolerance. Roots that have a greater cortical cell size may enhance plant growth under drought and nutrient stress (Chimungu et al. 2014; Lopez-Valdivia et al. 2023). An increased volume of individual cortical parenchyma cells, or the size of cortical cells, can decrease the metabolic costs of root growth and maintenance, in terms of both carbon costs of root respiration and the nutrient content of cortical tissue. For example, contrasting maize lines exposed to drought in the field or simulated under suboptimal nutrient availability with functional-structural plant models, demonstrated that plants with a larger cortical cell size had reduced respiration, deeper rooting, greater water and nitrogen uptake, and hence greater growth and yield (Chimungu et al. 2014; Lopez-Valdivia et al. 2023). The benefits of mycorrhizal colonization for enhanced plant nutrient and water status combined with greater cortical cell sizes that enhance soil foraging and stress tolerance may have synergistic effects for stress adaptation and enhanced yield.
While mycorrhizal fungi can mobilize plant molecular actors to alter the size and number of root cortical cells, it remains unclear how localized these responses are in the root. For example, these responses have been observed to be localized to only colonized cortical cells (Balestrini et al. 2007), but also at distal sites of the root and in both colonized and uncolonized cortical cells (Maldonado-Mendoza et al. 2005). While MIG1 and MIG2, and their homologues, may represent opportunities for enhanced stress adaptation, the benefit of altering cortical cell properties for enhanced stress tolerance will depend on the extent of these changes in cortical tissue within the entire root organ and if the magnitude of these benefits (or trade-offs) is enough to influence the metabolic cost of soil foraging and subsequently stress tolerance.
A better understanding of the trade-offs between root cortical traits and mycorrhizal fungi colonization in the root cortex may be useful for crop improvement
While a larger cortical cell size may promote the accommodation of arbuscular mycorrhizal fungi in cortical cells, other anatomical traits also influence the ability of colonization and hyphae growth and spread in the cortex. For example, root cortical aerenchyma can facilitate mycorrhizal spread as intercellular hyphae may benefit from a low-resistance path (i.e., air-filled lacunae) to grow through young roots (Brundrett et al. 1985; Brundrett and Kendrick 1987; Smith and Smith 1997). In maize inbred lines, increased arbuscular mycorrhizal colonization was associated with decreased aerenchyma formation (Galindo-Castañeda et al. 2019). However, in maize hybrid lines mycorrhizal colonization increased with larger aerenchyma lacunae, which coincided with larger root diameters (Galindo-Castañeda et al. 2019). Generally, mycorrhizal colonization occurs in living regions of the cortex not occupied by aerenchyma tissue with large, air-filled lacunae (Figs. 2 and 3) (Strock et al. 2019). In addition to its potential role in influencing mycorrhizal spread and spatial colonization, root cortical aerenchyma can improve abiotic stress tolerance. Aerenchyma can reduce the nutrient and respiratory demands of root tissues, reducing root metabolic costs that can translate into increased carbon allocation for deeper root growth and improved yield under suboptimal nutrient and water conditions (reviewed in Lynch et al. 2021). The interaction between root cortical aerenchyma formation and root mycorrhizal colonization, and their respective effect on plant hydromineral nutrient, remains to be further explored.
Similar to aerenchyma formation, the development of the anatomical trait, multiseriate cortical sclerenchyma, may also be an adaptation to improve soil foraging in edaphic stress. Multiseriate cortical sclerenchyma are characterized by small cell with thick cell walls encrusted with lignin in the outer cortex which enable plants to penetrate hard, dry soil and enhance soil foraging in deeper soil domains by increasing the tensile strength of the root (Schneider et al. 2021). However, mature palm root tissue with extensive cortical aerenchyma formation and sclerenchyma in the outer cortex showed reduced mycorrhizal colonization (Fig. 2) (Dreyer et al. 2010). Suberized and lignified apoplastic barriers in outer cortical tissue may reduce initial penetration of mycorrhiza into the root tissue and therefore reduce mycorrhizal colonization of the cortex (Sharda and Koide 2010). Further studies are required to understand the dynamics of these complex interactions between root anatomical traits and mycorrhizal colonization to unravel the benefits and trade-offs of these interactions for stress adaptation and enhanced yield.
Since both cortical traits and mycorrhizal fungi have the potential to improve plant hydro-mineral nutrition, the interplay of rhizosphere signals altering root cortical traits have the potential to have synergistic or potentially antagonistic interactions for soil resource acquisition and plant growth, particularly under drought and nutrient stress. We advocate for a comprehensive understanding of the benefits and trade-offs of root anatomical traits and root-rhizosphere interactions for plant growth in specific environments. The benefits of several anatomical traits for soil foraging and water and nutrient capture have been documented (as reviewed in Lynch et al. 2021), however the benefits and trade-offs of many of these traits on rhizosphere interactions in diverse environments remain to be explored. A cost-benefit optimization (i.e., applying microeconomic principles to plant resource allocation) may be used to determine the most beneficial plant (and rhizosphere) phenotypes in specific environments. Only after understanding the interplay between the root and rhizosphere can we identify optimal anatomical traits and root-rhizosphere interactions for improved plant performance in specific environments.
Perspectives and conclusions
Many opportunities remain to understand how developmental root and rhizosphere signals combine in the patterning of root cortical anatomy. For example, cortical cells colonized by arbuscular mycorrhizal fungi are not only typically larger in size, but also have thicker cell walls with altered cell wall characteristics including increased cellulose and hemicellulose content (Balestrini et al. 2005; Basyal and Emery 2021). While many of the molecular mechanisms of cell wall remodeling upon mycorrhizal signaling and colonization are unknown, several plant cell wall related genes have been shown to respond to symbiosis of mycorrhizal fungi (Balestrini and Bonfante 2014; Gutjahr et al. 2015). Thicker cell walls in cortical cells colonized by mycorrhizae may also be beneficial in edaphic stress. An increased proportion of volume occupied by energy-efficient compartments including vacuoles and cell walls can potentially reduce root metabolic cost and thereby plant fitness under conditions of drought, suboptimal nutrient availability, and soil mechanical impedance (Sidhu and Lynch 2024). We propose that arbuscular mycorrhizal fungi and plant developmental signals can frequently and extensively combine to alter root anatomy with potential synergistic interactions for enhanced nutrient efficiency.
A challenge to understanding root anatomy and rhizosphere interactions is the complexity of these interactions in time and space. Root exudation and nutrient, water, and oxygen concentration in the rhizosphere, and many other factors vary spatially and temporally on the root system. In addition, root anatomy depends on many factors including root class, tissue age, and root-microbe interactions (Canarini et al. 2019; Lynch et al. 2021; Salas-González et al. 2021). For example, the soil microbiome has been demonstrated to influence aerenchyma formation and endodermal suberization (Kawa et al. 2022). The integration of multiple root anatomical and architectural traits and rhizosphere characteristics may have synergistic or antagonistic effects for nutrient and water acquisition, pathogen resistance, and ultimately plant performance. In addition, consideration of dependency between anatomical and rhizosphere traits is important as the utility of specific traits can be masked by the integrated effects of multiple root and rhizosphere traits.
The influence of root anatomical and rhizosphere interactions on plant growth, health, and productivity are multifaceted and we must embrace this complexity to better define optimal phenotypes for specific environments. Because of these intricate complexities, it will be essential to study root anatomy and rhizosphere interactions on the same plant, rather than integrating information from distinct plants and systems. Due to the vast diversity of plant species and traits, microbiota, and growth environments a holistic approach is needed to study these interactions, emphasizing the importance of interdisciplinary collaboration among geneticists, microbiologists, agronomists, and computational biologists.
There is evidence that signals from the rhizosphere can mobilize plant molecular actors to modify the patterning and development of root anatomy. We highlight an example of this interplay describing how mycorrhizal fungi from the rhizosphere mobilize plant molecular actors controlling root anatomical traits including cortical cell size to facilitate their establishment and accommodation within the cortex. In addition, root anatomy and mycorrhizal fungi can have physical interactions in the cortex to promote or inhibit colonization. Research and breeding efforts targeting root anatomy to improve soil resource capture should consider microbial tradeoffs and microbial-root feedback that have the potential to modify or be modified by the root-rhizosphere environment. Understanding how roots and the rhizosphere interact is critical in mitigating impacts of abiotic and biotic stress on plant productivity.
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Acknowledgements
RB thanks Future Food Beacon and BBSRC Discovery (BB/S011102/1) Fellowships. AG thanks the Institut de Recherche pour le Développement for supporting this work. RJHS is funded by USDA Hatch Appropriations under Project #PEN04734 and Accession #1021929.
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Grondin, A., Li, M., Bhosale, R. et al. Interplay between developmental cues and rhizosphere signals from mycorrhizal fungi shape root anatomy, impacting crop productivity. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06611-z
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DOI: https://doi.org/10.1007/s11104-024-06611-z