Megan Ryan

• BA (ANU), BSc (hons) (ANU), PhD (ecology) (ANU)
• Professor at The University of Western Australia

The accumulation of soil organic matter (SOM) is influenced by the ecophysiological traits of soil microbes. Amending soils with stoichiometrically-balanced inputs can optimise microbial resource acquisition and subsequent carbon (C) stabilisation pathways. However, this mechanism has been poorly translated into practice. Wastewater biosolids can b...

Old cultivars or ecotypes of subterranean clover (Trifolium subterraneum) with concentrations of the isoflavone formononetin in green leaves greater than 0.20% of dry weight may reduce fertility and cause other health issues in sheep. Long-term pastures often develop diverse populations of subterranean clover, but there is little knowledge about th...

Societal Impact Statement Humans and honey bees have a long history of interaction to yield valued products and services. However, honey bees are under pressure from changes in vegetation, agricultural practices and climate change. We investigate if pasture legumes can be harnessed to support honey bees. We use a diverse set of species that origina...

Soil carbon supports desirable ecosystem functions for global agricultural productivity and climate resilience objectives. Wastewater biosolids can be transformed into soil amendments that return carbon and nutrients to agricultural systems in stoichiometric ratios that support carbon stabilisation. However, practicable delivery that enhances stabl...

Globally, agricultural land‐use negatively affects soil biota that contribute to ecosystem functions such as nutrient cycling, yet arbuscular mycorrhizal fungi (AMF) are promoted as essential components of agroecosystems. Arbuscular mycorrhizal fungi include Glomeromycotinian AMF (G‐AMF) and the arbuscule‐producing fine root endophytes, recently re...

Critical Zone Observatories (CZOs) are a global attempt to understand the function of the vertical ‘geo-bio-atmosphere boundary down to the bedrock’ critical zone (CZ) profile by characterising its physical, chemical and biological structure, learning how matter and energy are stored, transported and transformed within the CZ, and elucidating how t...

Recent evidence shows that the arbuscular mycorrhizal (AM) symbiosis is established by two distinct groups of fungi, with the distinctive fine root endophyte morphotype formed by fungi from the sub-phylum Mucoromycotina rather than the sub-phylum Glomeromycotina. While Mucoromycotina AM are abundant and globally distributed, there is currently no u...

High levels of the phytoestrogen formononetin (F) in green leaves of older cultivars (cvs) of subterranean clover (Trifolium subterraneum)-notably Dinninup, Dwalganup, Geraldton and Yarloop-can cause both transient and permanent fertility issues in ewes, as well as increased lamb and ewe mortality (known as clover disease). Cultivars bred for low F...

High levels of the phytoestrogen formononetin (F) in green leaves of older cultivars (cvs) of subterranean clover (Trifolium subterraneum)-notably Dinninup, Dwalganup, Geraldton and Yarloop-can cause both transient and permanent fertility issues in ewes, as well as increased lamb and ewe mortality (known as clover disease). Cultivars bred for low F...

Background Arbuscular mycorrhizas (AM) are the most widespread terrestrial symbiosis and are both a key determinant of plant health and a major contributor to ecosystem processes through their role in biogeochemical cycling. Until recently, it was assumed that the fungi which form AM comprise the subphylum Glomeromycotina (G-AMF), and our understan...

Phosphorus (P) recycling from wastewater can reduce the reliance on the primary source for P fertilisers―rock phosphate reserves. In light of this, we compared the effects of struvite (ST), a sparingly soluble P product derived from wastewater, and readily soluble KH 2 PO 4 (KP) on chickpea ( Cicer arietinum L.) and wheat ( Triticum aestivum L.) gr...

New markets for biosolids-derived products are urgently required to provide cost-effective solutions for water utilities to address the increasing production of municipal sewage waste. One potential outlet for biosolids is the domestic retail fertiliser market. Biosolids-derived fertilisers could be marketed to consumers by highlighting their envir...

Background Arbuscular mycorrhizas (AM) are the most widespread terrestrial symbiosis and are both a key determinant of plant health and a major contributor to ecosystem processes through their role in biogeochemical cycling. Until recently, it was assumed that the fungi which form AM comprise the subphylum Glomeromycotina (G-AMF), and our understan...

Cool temperatures can limit productivity of temperate grazing systems as poor pasture growth rates in winter create feed shortages for livestock. Ornithopus spp. (serradella) are broadly adapted annual pasture legumes that produce high-quality forage in soil types considered marginal for other temperate legume species. However, serradella establish...

The pasture legume Trifolium subterraneum ssp. yanninicum L. is waterlogging tolerant, but water‐deficit (WD) susceptible. The interactive effect of waterlogged (WL) and WD (soil moisture fluctuation [SMF]) results in a severe stress impact. We studied three diverse ecotypes to identify traits associated with adaptation to SMF. Ecotypes were establ...

Images of roots colonised by M-AMF and G-AMF

Current literature suggests ecological niche differentiation between co-occurring Mucoromycotinian arbuscular mycorrhizal fungi (M-AMF) and Glomeromycotinian AMF (G-AMF), but experimental evidence is limited. We investigated the influence of soil age, water availability (wet and dry), and plant species (native Microlaena stipoides and exotic Trifol...

The isoflavone formononetin (F) impacts livestock fertility and cultivars of the pasture legume Trifolium subterraneum L. (subclover) have been selected for F levels ≤0.2% of leaf dry weight. However, the impact of waterlogging (WL) on isoflavones is little studied. We investigated the response of isoflavones, biochanin A (BA), genistein (G) and F,...

The use of acid soil-tolerant annual legume pasture species and liming to raise soil pH can have legacy effects that improve subsequent wheat crop growth in acid soils. We established a two-year experiment in a semi-arid environment with and without historical lime application to investigate how acid soils (±lime) influence the legacy effects of an...

The coordination/trade-off among below-ground strategies for phosphorus (P) acquisition, including root morphology, carboxylate exudation and colonisation by arbuscular mycorrhizal fungi (AMF), is not well understood. This is the first study investigating the relationships between root nodulation, morphology, carboxylates, and colonisation by an in...

In brief Dietary phytoestrogens disrupt a specific stage of ram spermatogenesis, causing subtle decreases in sperm quality by affecting the expression of pathways involved in the structural integrity of the spermatozoa. This paper demonstrates for the first time that ram reproduction is compromised by oestrogenic pasture, whilst also providing a lo...

Purpose Root exudation of organic acids (OAs) facilitates plant P uptake from soil, playing a key role in rhizosphere nutrient availability. However, OA exudation responses to CO2 concentrations and water availability remain largely untested. Methods We examined the effects of CO2 and water on OA exudates in three Australian woodland species: Euca...

This paper reviews the distribution and importance of annual clover (Trifolium) species forpasture and fodder production systems globally. Of the 158 recorded annual Trifolium species, 65.2%are endemic to the Mediterranean basin and surrounding areas, 14.6% to sub-Saharan Africa, 17.7%to the United States of America and 2.5% to Chile. Fourteen spec...

Although significant intraspecific variation in photosynthetic phosphorus (P)-use efficiency (PPUE) has been shown in numerous species, we still know little about the biochemical basis for differences in PPUE among genotypes within a species. Here, we grew two high-PPUE and two low-PPUE chickpea (Cicer arietinum) genotypes with low P supply in a gl...

Leaf phosphorus (P) comprises four major fractions: inorganic phosphate (Pi), nucleic acids, phospholipids, P‐containing metabolites and a residual fraction. In this review paper, we investigated whether allocation of P fractions varies among groups of terrestrial vascular plants, and is indicative of a species' strategy to use P efficiently. We fo...

Subterranean clover (subclover, Trifolium subterraneum L.), is the most widely sown annual pasture legume in southern Australia, but winter waterlogging can cause extensive biomass reductions. Determining an efficient and non-destructive screening method for waterlogging tolerance is crucial for subclover breeding programs to identify parents and p...

Harvesting subterranean clover seed is technically challenging and is reliant on suction harvesters developed in the early 1960s. Current challenges with the cost, difficulty and environmental impacts of seed harvesting threaten the future of the seed production industry. To overcome these challenges, we are investigating the use of peanut harvesti...

Many plant species from regions with ancient, highly-weathered nutrient-depleted soils have specialised adaptations for acquiring P and are sensitive to excess P-supply. Mycorrhizal associations may regulate P-uptake at high external P-concentrations, potentially reducing P-toxicity. We predicted that excess P-application will negatively impact spe...

Background and aims This study investigated whether root traits at the seedling stage are maintained at the flowering stage in two chickpea (Cicer arietinum) genotypes with contrasting root morphology and physiology; and whether the genotype with greater rhizosheath carboxylates mobilises more poorly-available phosphorus (P) pools to increase shoot...

Purpose: Root exudation of organic acids (OAs) facilitates plant P uptake from soil, playing a key role in rhizosphere nutrient economy. However, OA exudation responses to elevated CO2 concentrations (eCO2) and water availability remain largely untested. Methods: We examined the interactive effects of CO2 and water on OA exudates in three Australia...

Background and aims The pasture legume Trifolium subterraneum ssp. yanninicum exhibits waterlogging tolerance. This study investigates diversity for waterlogging tolerance within ssp. yanninicum . We tested the hypotheses that (1) variation for waterlogging tolerance exists within ssp. yanninicum and (2) is related to phenotypic and growth trait di...

Background Soils harbour a remarkable diversity of interacting fungi, bacteria, and other microbes: together these perform a wide variety of ecological roles from nutrient cycling and organic matter breakdown, to pathogenic and symbiotic interactions with plants. Many studies demonstrate the role of microbes in plant-soil feedbacks and their intera...

Farmers are often overlooked and undervalued as sources of innovation, but can be powerful drivers of ingenuity and development. We evaluate historical developments in the Australian subterranean clover seed-production industry as a case study of farmer-driven innovation. Subterranean clover seed machinery patents (75% of which were patented by far...

Food waste can be used via anaerobic digestion (AD) to produce biogas. The liquid by-product (digestate) contains nitrogen (mainly as ammonium) which is susceptible to N loss as a fertiliser and also faces logistical constraints for agricultural use. Biochar can adsorb and retain nutrients and alter microbial N-cycling processes. We investigated th...

Trifolium subterraneum L. subsp. yanninicum is a pasture legume that is widely grown in medium and high rainfall areas of southern Australia and shows waterlogging tolerance. This study investigated diversity within subsp. yanninicum corresponding to eco-geographic variables, which may help to identify adapted parents with new traits for genetic im...

Seed retention has not been evaluated for subterranean clover ( Trifolium subterraneum L.), because its geocarpic seed-bearing burrs are currently harvested by suction systems. Development of improved harvest methods requires knowledge of subterranean clover seed retention characteristics and their changes with plant development. This study evaluat...

Many plant species from regions with ancient, highly-weathered nutrient-depleted soils have specialised adaptations for acquiring P and are sensitive to excess P-supply. Mycorrhizal associations may regulate P-uptake at high external P-concentrations, potentially reducing P-toxicity. We predicted that excess P-application will negatively impact spe...

Background and AimsIn the annual pasture legume Trifolium subterraneum , ssp. yanninicum exhibits higher waterlogging tolerance than ssp. brachycalycinum and ssp. subterraneum . This study investigates waterlogging tolerance within ssp. yanninicum ecotypes and explores correlations with seedling phenotypic traits and site of origin eco-geographic v...

With a growing population and changing climate, there is an urgent need to increase global agricultural yields, while minimizing environmental impacts and land use. A component of this “sustainable intensification” process is the shift from synthetic fertilizer to nitrogen-fixing legumes. Subterranean clover (Trifolium subterraneum L.) is the world...

Aims：Plants deploying a phosphorus (P)-mobilising strategy via carboxylate release have relatively high leaf manganese concentrations ([Mn]). Thus, leaf [Mn] is a proxy for the amount of rhizosheath carboxylates. Whether the concentrations of other leaf micronutrient, such as iron ([Fe]), zinc ([Zn]) and copper ([Cu]), show a similar signal for rhi...

Differences in root morphology and acclimation to low‐phosphorus (P) soil were examined among eight legume species from the Trifolium Section Tricocephalum to understand how these root attributes determine P acquisition. Ornithopus sativus was included as a highly P‐efficient benchmark species. Plants were grown as microswards in pots with five rat...

The Kimberley region of Western Australia is a National Heritage listed region that is internationally recognised for its environmental and cultural significance. However, petroleum spills have been reported at a number of sites across the region, representing an environmental concern. The region is also characterised as having low soil nutrients,...

Messina (Melilotus siculus) cv. Neptune, an annual pasture legume native to the Mediterranean Basin, has recently been released for saltland pastures in southern Australia following demonstration of biomass production and persistence superior to other commercial pasture legumes in saline environments prone to winter waterlogging. Self-regenerating...

Subterranean clover (Trifolium subterraneum) was probably introduced into Western Australia in the 1830s and has since become integral to pasture systems across southern Australia (Nicholls et al. 2013). In the 1940s, it was linked to severe infertility in sheep, 'clover disease' (Bennetts et al. 1946). The causative agent was found to be a group o...

Subterranean clover (Trifolium subterraneum L) is the dominant annual pasture legume in southern Australia (30 million ha) and is an essential part of the livestock industry. Reproductive difficulties in sheep grazing subclover pastures high in oestrogenic compounds were first described in the 1940s (Bennetts et al. 1946). Oestrogenic subclovers ca...

Chickpea—the second most important grain legume worldwide—is cultivated mainly on marginal soils. Phosphorus (P) deficiency often restricts chickpea yields. Understanding the genetics of traits encoding P-acquisition efficiency and P-use efficiency will help develop strategies to reduce P-fertilizer application. A genome-wide association mapping ap...

Fine root endophytes (FRE) were traditionally considered a morphotype of arbuscular mycorrhizal fungi (AMF), but recent genetic studies demonstrate that FRE belong within the subphylum Mucoromycotina, rather than in the subphylum Glomeromycotina with the AMF. These findings prompt enquiry into the fundamental ecology of FRE and AMF. We sampled FRE...

AimsTolerance to waterlogging and recovery ability was compared among the three subspecies of subterranean clover (Trifolium subterraneum L.) to identify tolerance mechanisms, in order to guide future subclover breeding activities.Methods Three cultivars each of ssp. yanninicum, subterraneum and brachycalycinum were grown in a controlled environmen...

Subterranean clover (Trifolium subterraneum L.) is Australia’s most widely sown annual pasture legume. Its widespread use as a pasture plant requires a well-functioning seed production industry, and Australia is the only significant producer of subterranean clover seed globally. However, the sustainability of this industry is under threat due to it...

Subterranean clover (Trifolium subterraneum L.) and annual medics (Medicago spp.) are Australia's most widely sown pasture legumes and the continued importance of these species requires a well-functioning seed production industry. However, harvesting their seed presents significant practical challenges. Sixty-year-old technology is still used to ha...

Aims We investigated the effects of water stress under low phosphorus (P) supply on P-acquisition by chickpea, and identified a genotype with faster relative growth and P-acquisition rates. Methods We grew four genotypes in pots filled with a sand and soil mixture with a low P availability in a glasshouse. Plants were either well-watered or water...

Serradella (Ornithopus) species are high‐quality pasture legumes that originate from the Mediterranean basin and have been increasingly used in southern Australian temperate grazing systems. They are generally regarded as tolerant of soils with low pH and, by inference, elemental toxicities such as aluminium (Al). No studies have examined the effec...

At a global scale, phosphorus (P) deficiency comprises a large area of cropland, while P has also been used in excess of crop requirements in many other regions. Improved crop P-acquisition efficiency would allow lower target critical soil P values and provide savings in P-fertiliser use. At the same time, it would reduce P lost through erosion, le...

Ptilotus exaltatus accumulates phosphorus (P) to > 40 mg g-1 without toxicity symptoms, while Kennedia prostrata is intolerant of increased P supply. What physiological mechanisms underlie this difference and protect P. exaltatus from P toxicity? Ptilotus exaltatus and K. prostrata were grown in a sandy soil with low-P, high-P and P-pulse treatment...

Aims Arbuscule-producing fine root endophytes (FRE) (previously incorrectly Glomus tenue) were recently placed within subphylum Mucoromycotina; the first report of arbuscules outside subphylum Glomeromycotina. Here, we aimed to estimate nutrient concentrations in plant and fungal structures of FRE and to test the utility of cryo-scanning electron m...

AimsThis study aimed to determine the structure of the bacterial community inhabiting the roots and rhizosheath of sweet potato cultivars, and how these bacterial communities respond to P addition and subsequent changes in carboxylate exudation by sweet potato roots.Methods Five sweet potato cultivars were grown with and without P addition in a low...

The challenges facing global agriculture via population increase, climate change and dietary choices are unprecedented and urgent. In the context of declining public funding for research and development in agriculture (ag R&D), we highlight the historically high returns on such investments and outline an economic rationale to continue government in...

Fertiliser application to restore nutrients lost in the mining process and facilitate early plant establishment and growth is a key step in the restoration of sites disturbed by mining. However, few studies have investigated the effects of different fertiliser types and application methods on mine restoration outcomes, especially in highly biodiver...

Increasing the area sown to Ornithopus spp. (serradella) can reduce overall fertiliser requirements in Australian permanent pastures owing to their greater nutrient-acquisition efficiency than that of more widely used pasture legumes such as Trifolium spp. However, uncertainty regarding waterlogging tolerance of Ornithopus spp. may restrict their a...

Species in the Australian genus Ptilotus (Amaranthaceae) grow well in soils with both very low and very high phosphorus (P) availability; in the latter they hyperaccumulate P. However, it is not known whether this trait is common within Ptilotus, whether it is shared with other genera in the family, or whether it correlates with the wide array of m...

Adjustments in root biomass allocation, root morphology, carboxylate exudation and mycorrhizal symbiosis are well‐known strategies for plants to cope with phosphorus (P) deficiency. Large genotypic variation in these functional traits has been demonstrated within numerous species. Yet, whether these functional traits are coordinated differently amo...

The development of early warning indicators that identify ecosystem stress is a priority for improving ecosystem management. As microbial communities respond rapidly to environmental disturbance, monitoring their composition could prove one such early indicator of environmental stress. We combined 16S rRNA gene sequencing of the seagrass root micro...

Plant growth on harsh substrates (habitat specialization) requires specific traits to cope with stressful conditions. We tested whether traits related to nutrient acquisition (root colonization by fungal symbionts, and plant morphological and physiological specializations), and nutrient use (leaf nitrogen (N) and phosphorus (P) concentrations and N...

In recent decades several pasture legumes have been available in southern Australia as potential alternatives to the most widely used annual pasture legume Trifolium subterraneum. Little is known about their soil phosphorus (P) requirements, but controlled environment experiments indicate that at least some may differ in their P fertiliser requirem...

Plants invest their carbon resource in various strategies to enhance phosphorus (P) uptake and use when growing in low P soils. Sweet potato has evolved and persisted in P-impoverished soils, but exhibits highly variable growth and yield. Variation among sweet potato cultivars in ability to access and use P may affect growth and yield: the influenc...

Plant roots exhibit diverse root functional traits to enable soil phosphorus (P) acquisition, including changes in root morphology, root exudation and mycorrhizal symbioses. Yet, whether these traits are differently coordinated among crop species to enhance P acquisition is unclear. Here, eight root functional traits for P acquisition were characte...

Crops with improved uptake of fertiliser phosphorus (P) would reduce P losses and confer environmental benefits. We examined how P‐sufficient six‐week‐old soil‐grown Trifolium subterraneum plants, and two‐week‐old seedlings in solution culture, accumulated P in roots after inorganic P (Pi) addition. In contrast to our expectation that vacuoles woul...

We welcome the comments of Rillig et al. (2018) on Ryan & Graham (2018). A robust debate concerning the need to manage arbuscular mycorrhizal fungi (AMF) in agricultural systems has been long overdue. We agree with Rillig et al. (2018) that AMF can play an important role in many processes that may benefit the functioning and yield of agricultural s...

Crops with improved uptake of fertiliser phosphorus (P) would reduce P losses and confer environmental benefits. We examined how P-sufficient six-week-old soil-grown Trifolium subterraneum plants, and two-week-old seedlings in solution culture, accumulated P in roots after inorganic P (Pi) addition. In contrast to our expectation that vacuoles woul...

Understanding the mechanisms that underlie the generation of beta‐diversity remains a challenge in ecology. Underground plant adaptations to environmental gradients have received relatively little attention. We studied plant nutrient‐acquisition strategies and nutrient‐use efficiency at three stages of pedogenesis in infertile soils from campos rup...

Fertilizers are a significant input cost (range from 20 to 30%) of grain production in Australia. Phosphorus (P) is the second most important nutrient for plant growth and modern agricultural production systems rely on its application. Therefore, an accurate estimate of P application and plant– soil interactions that enhance P availability to plant...

Seagrasses thrive in anoxic sediments where sulphide can accumulate to phytotoxic levels. So how do seagrasses persist in this environment? Here, we propose that radial oxygen loss (ROL) from actively growing root tips protects seagrasses from sulphide intrusion not only by abiotically oxidising sulphides in the rhizosphere of young roots, but also...

The bioremediation of historic industrial contaminated sites is a complex process. Co-contamination, often with lead which was commonly added to gasoline until 16 years ago is one of the biggest challenges affecting the clean-up of these sites. In this study, the effect of heavy metals, as co-contaminant, together with total petroleum hydrocarbons...

Contents Summary I. Introduction II. Investigating activity of AMF in agroecosystems III. Crop benefit from AMF: agronomic and mycorrhizal literature differ IV. Flawed methodology leads to benefits of mycorrhizas being overstated V. Rigorous methodology suggests low colonisation by AMF can sometimes reduce crop yield VI. Predicting when mycorrhizas...

In recent years there has been great progress with the implementation and utilization of Clustered Regularly Interspaced Palindromic Repeats (CRISPR) and CRISPR-associated protein (Cas) systems in the world of genetic engineering. Many forms of CRISPR-Cas9 have been developed as genome editing tools and techniques and, most recently, several non-ge...

Root foraging and root physiology such as exudation of carboxylates into the rhizosphere are important strategies for plant phosphorus (P) acquisition. We used 100 chickpea ( Cicer arietinum ) genotypes with diverse genetic backgrounds to study the relative roles of root morphology and physiology in P acquisition. Plants were grown in pots in a low...

Improving phosphorus (P)-use efficiency in legumes is a worldwide challenge in the face of an increasing world population, dwindling global rock phosphate reserves, the relatively high P demand of legumes and global change. This review focuses on P acquisition of crop legumes in response to climate change. We advocate further studies on: firstly, t...

AimsLow-molecular-weight organic anions (carboxylates) influence rhizosphere processes and may enhance plant phosphorus acquisition. We examined the root exudate profile of a range of pasture and grain legumes and focused on the little-investigated carboxylate, citramalate. Methods Twelve species of pasture legumes and herbs, including four Lotus s...

Background and aimsThe growth and root morphology responses to soil phosphorus (P) fertility by five cultivars of Trifolium subterraneum (a temperate annual pasture legume) were examined to assess whether differences in root morphology and/or root acclimation to P stress influenced P-acquisition by the clover varieties, or their critical P requirem...

During long-term ecosystem development and its associated decline in soil phosphorus (P) availability, the abundance of mycorrhizal plant species declines at the expense of non-mycorrhizal species with root specialisations for P-acquisition, such as massive exudation of carboxylates. Leaf manganese (Mn) concentration has been suggested as a proxy f...

Annual pasture legumes with a superior ability to acquire soil phosphorus (P) and a low external critical P requirement could reduce the need for P fertiliser. Roots of pasture legumes grown in field soil will commonly be colonised by arbuscular mycorrhizal fungi (AMF). However, recent research suggests a second community of arbuscule-forming root-...

The mainstream pasture legume species such as Trifolium subterraneum, T. repens and annual Medicago spp. used in the temperate pasture systems of southern Australia have high critical external requirements for phosphorus (P) (i.e. P required to achieve 90% of maximum yield). This work aimed to identify alternative pasture legume species that could...

Seagrass roots host a diverse microbiome that is critical for plant growth and health. Composition of microbial communities can be regulated in part by root exudates, but the specifics of these interactions in seagrass rhizospheres are still largely unknown. As light availability controls primary productivity, reduced light may impact root exudatio...