A tribute to Sally E. Smith

Francis Martin, Ian Dickie, Bjorn D. Lindahl, Sarah Lennon, Maarja Öpik,
Andrea Polle, Natalia Requena, Marc-André Selosse, Roger T. Koide, Iver
Jakobsen, et al.

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To cite this version:

Francis Martin, Ian Dickie, Bjorn D. Lindahl, Sarah Lennon, Maarja Öpik, et al. A tribute to Sally E. Smith. New Phytologist, 2020, 228 (2), pp.397-402. 10.1111/nph.16895. hal-02990560

HAL Id: hal-02990560

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Editorial

A tribute to Sally E. Smith

Prof. Sarah (Sally) E. Smith, a long-standing *New Phytologist*
Advisory Board member, and friend to the journal, died in
September 2019. Sally will be remembered not only for her
outstanding body of work, but for her friendship, mentorship and
leadership of the mycorrhizal research community. By way of
tribute we invited colleagues of Sally to share their recollections,
and we publish this Virtual Issue in her memory.

Sally was born in 1941, and received Bachelor and PhD degrees
from Cambridge University, UK, before relocating to Adelaide,
Australia in the late 1960s, alongside her husband Andrew (FA)
Smith. Upon arrival in Adelaide, Sally undertook a number of
positions at the University of Adelaide's Botany Department,
followed by research work at the Waite Research Institute. In 1991
she was appointed Senior Lecturer in the Department of Soil
Science, and she received a Doctorate of Science from the University
of Adelaide that same year. Sally was appointed Professor in 1995.

Sally was elected a Fellow of the Australian Academy of Science in 2001, and, among numerous awards, she received an Australian Centenary Medal for contribution to Australian society and services to biology (2003), the Taylor (2006) and Prescott (2012) medals of the Australian Society of Soil Science, and the International Mycorrhiza Society's Eminent Mycorrhiza Researcher Award (2019). Sally was also Honorary Professor at the Research Centre for Eco-Environmental Sciences (Chinese Academy of Sciences), and an Honorary Research Professor at the Chinese Agricultural University, Beijing.

Sally officially retired in 2006, but remained very active, holding
an Adjunct and later Emeritus Chair at the University of Adelaide,
contributing to many international meetings, including the 2014,
33rd *New Phytologist* Symposium 'Networks of Power and
Influence: Ecology and Evolution of Symbioses between Plants
and Mycorrhizal Fungi' (Bender *et al*, 2014), and continuing to act
as an Advisory Board Member at *New Phytologist*, providing much-
valued critical insight and advice to our Editors. Her reviews, even
when she disagreed, were always supportive and positive; she often
provided much detailed advice and her large view of the literature to
the authors.

In January 2019, *New Phytologist* published a Profile of Sally (Smith, 2019), which outlines her achievements in more detail, but importantly, it also highlights her many personal qualities. In the profile, Sally outlined the successes and challenges she faced throughout her career, but she also dwells on the many friendships and relationships she developed; her warmth, and generosity, is evident throughout the piece, and also in the personal recollections outlined below (Fig. 1).

In a way, Sally is still here with us. We are still prepared to hear
her unforgettable voice at conferences; we still use the precious and
irreplaceable textbook ‘*Mycorrhizal symbiosis*’ she wrote with David

<figure><img src="image_4.png" /><figcaption>**Fig. 1** The photograph of Sally E. Smith featured in her 2019 profile. This photograph was later used in a banner as part of a state-wide celebration of the 125th anniversary of female suffrage in South Australia. Sally was featured as one of 46 eminent women associated with the University of Adelaide.</figcaption></figure>

Read, which will forever remind us of the first steps of our research
community and the broad view she had of the symbiosis (Smith &
Read, 2008). Sally will be greatly missed, as a scientist, friend,
colleagues and mentor.

Acknowledgements

We are very grateful to Andrew Smith for his support of this Virtual
Issue and for his help in compiling the text.

ORCID

Sarah Lennon [ID] https://orcid.org/0000-0002-2860-6480
Björn D. Lindahl [ID] https://orcid.org/0000-0002-3384-4547
Francis M. Martin [ID] https://orcid.org/0000-0002-4737-3715
Maarja Öpik [ID] https://orcid.org/0000-0001-8025-7460
Andrea Polle [ID] https://orcid.org/0000-0001-8697-6394
Marc-André Selosse [ID] https://orcid.org/0000-0003-3471-9067

Francis M. Martin* [ID]

Lab of Excellence ARBRE, UMR 1136 INRA-Université de
Lorraine 'Interactions Arbres/Micro-organismes', INRAE,
54280 Champenoux, France

Ian Dickie

College of Science, University of Canterbury, Private Bag 4800,
Christchurch 8140, New Zealand

Björn D. Lindahl [ID]

Department of Soil and Environment, Swedish University of
Agricultural Sciences, Box 7014, 750 07 Uppsala, Sweden

Sarah Lennon [ID]

New Phytologist Central Office, Bailrigg House, Lancaster
University, Lancaster, LA1 4YE, UK
Maarja Öpik ID

Department of Botany, Institute of Ecology and Earth Sciences,
University of Tartu, 40 Lai St 51005 Tartu, Estonia

Andrea Polle ID

Department of Forest Botany and Tree Physiology, Buesgen-
Institute and Göttingen Center for Molecular Biosciences
(GZMB), University of Göttingen, Göttingen 37077, Germany

Natalia Requena

Molecular Phytopathology Department, Karlsruhe Institute of
Technology, Fritz Haber-Weg 4, Geb. 30.43, 2. OG D-76131,
Karlsruhe, Germany

Marc-André Selosse ID

Département Systématique et Evolution, UMR 7205 ISYEB
CP 50, Muséum national d'Histoire naturelle, 45 rue Buffon,
Paris 75005, France
Faculty of Biology, University of Gdansk, ul. Wita Stwosza 59,
80-308 Gdansk, Poland

(*Author for correspondence email: francis.martin@inrae.fr)

Sarah Elizabeth 'Sally' Smith: 'no microphone required', by Roger Koide

At more than one conference, Sally announced to her audience that her voice was naturally of sufficient volume that she didn't need a microphone. It is equally true that the impact of her research and the influence she had on her many colleagues and students are truly impressive without additional amplification.

Sally was my host during a 6-month sabbatical in 1992 at the Waite Research Institute of the University of Adelaide. My wife, three children and I arrived in Adelaide to a furnished home that Sally had arranged for us to rent and her daughter's car for us to use until we could arrange our own transport. She showed us many such kindnesses as I am sure she has for countless others. Later, when she came for a visit to Penn State University, rather than waste time chatting with me, she immediately sought out my students,<fnref n="1" /> making herself useful by helping to sort plant samples. I will always remember her as a woman ready, willing and able to help.

Considering her large contributions to the understanding of
arbuscular mycorrhizal symbioses, many of you may be surprised
to learn that Sally did not have the advantage of a conventional
academic career. After earning her PhD on orchid mycorrhiza
physiology in 1965 and publishing her first two papers in 1966
and 1967, there were no other publications until 1977. In the
intervening years Sally was busy raising two daughters and
holding various temporary teaching positions, and there was
little opportunity for research. Collaborations were instrumental
in restarting Sally's research career; her third, fourth and fifth
publications resulted from collaborations with Melvin Daft
(Smith & Daft, 1977), Andrew Smith (Smith *et al.*, 1979) and
Glyn Bowen (Smith & Bowen, 1979), marking a fateful shift to
the study of arbuscular mycorrhizas. As an expert on orchid *and*
arbuscular mycorrhizas, it made sense in the early 1980s for

Sally's father, Jack Harley, to ask her to co-author the first
edition of *Mycorrhizal Symbiosis* (Harley & Smith, 1983)
Throughout the 1980s other significant research was initiated
(e.g. Smith & Gianinazzi-Pearson, 1988), all before her first
permanent academic position in 1991 in the Department of
Agricultural Biochemistry at the Waite.

Australia is plagued by some of the most phosphorus (P)-
deficient soils on earth (Lambers et al., 2013), and there are three
times as many sheep in Australia as there are people. Not
surprisingly, much of Sally's research concerned the impact of
arbuscular mycorrhizal fungi (AMF) on uptake of P by forage crops
such as alfalfa and subterranean clover. In much of Sally's research,
there is a clear progression from the description of broad
phenomena to the understanding of specific mechanisms that
explain those phenomena. For example, Sally and her students
quantified with great care the transfer of P from fungus to root
(Smith, 1982; Smith & Dickson, 1991) and, subsequently, the
anatomical, physiological and genetic mechanisms responsible for
those transfers (Gianinazzi-Pearson & Smith, 1991; Smith et al.,
1994; Murphy et al., 1997; Ezawa et al., 2001a,b, 2004; Smith &
Barker, 2002; Glassop et al., 2007; Rosewarne et al., 2007,
Rosewarne et al. 1999; Manjarrez et al., 2010).

Sally and her students also described how mycorrhizal fungal
colonization is influenced by various aspects of the physical
environment, including light (Tester et al., 1986; Son & Smith,
1988), P availability (Smith, 1982), temperature (Baon et al.,
1994), fertilizer ions (Chambers et al., 1980), propagule concen-
tration (Walker & Smith, 1984), fallow (Haugen & Smith, 1992)
and soil compaction (Nadian et al., 1996). Subsequently, they
investigated the genetic, physiological, cellular and anatomical
considerations in the establishment of symbiosis (Smith et al.,
1992; Bruce et al., 1994; Barker et al., 1998; Rosewarne et al.,
2007).

Phosphorus transport would always be of major interest to
Sally, but it would always be placed within the context of the
entire physiological interdependence between plant and fungus.
Indeed, Sally maintained an interest in the carbon economy of
the host plant as influenced by the fungus (Silsbury et al., 1983)
and in the flow of carbon from host to fungus (Manjarrez et al.,
2008).

Although at heart a physiologist, Sally appreciated the ecological
context in which all organisms existed. Consequently, she and her
students and colleagues studied the significant variation that exists
among communities of AMF species in their morphology (Cav-
agnaro et al., 2001; Dickson et al., 2007), colonization phenotype
(Gao et al., 2001), their ability to colonize roots from a distance
(Drew et al., 2006), their ability to acquire P from soil (Cavagnaro
et al., 2005), their propensity to transfer P to host plants (Smith
et al., 2000), and in their capacity to mine soil at a variety of
distances from the root (Jansa et al., 2008). They also studied
mycorrhizal fungal dispersal mechanisms (Pattinson et al., 1997)
and the role played by arbuscular mycorrhizal fungi in soil
aggregation (Tisdall et al., 1997), plant competition (Facelli et al.,
1999) and plant diversity and community structure (O'Connor
et al., 2002; Lambers et al., 2008).

<footnote n="1">¹Editor's note: *New Phytologist* Editor Ian Dickie feels fortunate to have been one of these students.</footnote>
Sally authored or co-authored several choice review articles. My favorite is the review on structural diversity in AM symbiosis (Smith & Smith, 1997). And, of course, the three editions of *Mycorrhizal Symbiosis* (Harley & Smith, 1983; Smith & Read, 1997, 2008) have educated multiple generations of scholars.

Sally's many direct contributions to our field are highly significant. But her greatest impact may be indirect, stemming from the many individuals she influenced for good. Generations of undergraduate and postgraduate students, postdoctoral researchers and local and international colleagues owe much to Sally Smith. *Goodonya, Sal*.

Roger T. Koide ID

Department of Biology, Brigham Young University, Provo, UT
84602, USA

## A tribute to Sally Smith, by Iver Jakobsen

With the passing of Sally Smith, the world of science and of mycorrhizal research, in particular, has lost an outstanding and passionate expert, teacher and role model; her impact on our current understanding of mycorrhizal functioning cannot be overstated. This tribute to Sally is based on three decades of research collaboration that developed into a deep friendship.

Back in 1990, I visited Sally in Adelaide together with my family and was struck by Sally's impressive knowledge on mycorrhizas, by her very intense and constructive scientific support and by her great hospitality. Thereby, a foundation was established for several later research collaborations and exchanges of students. Together with her husband and colleague Andrew Smith, Sally came to conduct experimental work in my lab on three occasions to use radioisotopes to enhance our understanding of phosphorus uptake in arbuscular mycorrhizas. The work resulted in the development of a now widely used model system that enables the determination of the fungal contribution to overall plant P uptake. This successful collaboration was largely driven by the enthusiasm and energy that Sally brought to and disseminated in the lab. Everyone, at all levels, enjoyed working with Sally due to her thoughtful and timely approaches. Sally eagerly monitored all possible plant variables during an experiment, and she was likewise the main driving force and active participant during plant harvest as well as data collection and analyses. Her eminent writing skills always ensured that novel findings got published in prominent journals.

Everybody in the lab looked forward to visits by Sally, because she so generously spread her enthusiasm, inspiration and support in a straightforward, yet passionate, empathetic and friendly manner. It was a pleasure to experience her active and constructive contributions at lab meetings and seminars. Furthermore, Sally truly cared about the younger scientists and became an invaluable mentor for students, who were always excited to be invited to visit Sally's lab. In return, we were lucky to also host several of Sally's excellent students on experimental research visits.

In conjunction with her world-recognized contributions to science, Sally had a positive impact on the Danish research environment by her active participation in the evaluation of proposals for a major national granting foundation.

Collaborating with Sally developed into a good friendship. It was always enjoyable and with a lot of cheerful laughter when she and Andrew came to visit. Her sense of humour and lively reports from their daily life and many bird-watching trips contributed to the joy. Sally will be missed in Denmark.

Iver Jakobsen ID

Plant and Environmental Sciences, University of Copenhagen,
Thorvaldsensvej 40,1871, Frederiksberg C, Denmark

## Sally Smith: more than a mentor – a sponsor and friend

Sally's research output is extraordinary. Here we focus on Sally's work from 2000 and onwards, but it is worth noting that in a comprehensive search for published works we encountered 82 papers pre-2000. The period 2000–2009 was a time when the Smith lab was busy with PhD students, Postdocs and visitors, and the first decade of the 2000s alone saw a further 91 papers co-authored by Sally, many of which saw her as senior author. The quality and impact of Sally's work is highlighted by her repeated inclusion (more than a decade after her official retirement) in *Web of Science*'s Highly Cited Researcher list.

Much of Sally's research focused on understanding how arbuscular mycorrhizal fungi transport phosphorus (P) to the host plant, and on questions of function surrounding this important role. A major influence on this was the ongoing collaboration Sally (and Andrew Smith) had with Prof. Iver Jakobsen's lab (then at the Technical University of Denmark, which is outlined above).

Sally and her collaborators' findings on P uptake spurred further work to discover the underlying cause of 'non-responsive' plants, such as wheat and barley, which included comprehensive studies of fungal biomass, mycorrhizal pathway (MPU) activity and phosphate transporter (PT) gene expression (Li et al., 2008; Grace et al., 2009; Smith et al., 2009). Indeed, Sally's work at the Waite campus of the University of Adelaide (an agricultural research hub) was often geared towards answering fundamental questions, but generally came with a broader agricultural applicability. Her lab's comprehensive work on how crop P-efficiency related to AMF in different varieties of wheat (Zhu et al., 2001a,b,c, 2006; Li et al., 2005, 2006), rice (Geng et al., 2005; Glassop et al., 2007), buckwheat (Zhu et al., 2002a), and barley (Zhu et al., 2002b, 2003; Li et al., 2003), challenged the tightly held beliefs of many that AMF do not have a role to play in field crops. A key feature of this work is the way in which Sally combined different threads of information (gene expression, whole plant physiology, etc.) to discover underlying processes and mechanisms, and their significance.

Many of Sally's students and Postdocs continued to explore radioisotopes and the MPU, including the use of radioisotopes to discover how AM fungal functional diversity works to explore P patches in soil (Cavagnaro et al., 2005), and to understand how phosphate transporters and their encoding genes interact with the MPU (Glassop et al., 2005). More recently, P radioisotopes have been used in Sally's extended lab group to test the effect of carbon (C) limitation on AMF contribution to plant P (Stonor et al., 2014). This work was undertaken to demonstrate the P contribution to wheat in the field (Smith et al., 2015), and to explore the
interaction between AMF interactions with elevated CO2 and P availability (Jakobsen et al., 2016).

The identification and characterization of a tomato mutant with a reduced mycorrhizal colonization (rmc) phenotype changed how Sally's lab approached questions on the mycorrhizal symbiosis, and how experiments should be conducted. Now, instead of relying on a sterilised growth substrate to act as the 'nonmycorrhizal control' (a sticking point with many reviewers, still), there was scope to grow the mutant and wild-type tomato plants in nonsterile field soil with the indigenous microbial (including AMF) community. Sally's lab rigorously tested the rmc mutant, both to ensure its suitability as a nonmycorrhizal control (Gao et al., 2002; Cavagnaro et al., 2004a,b), and to discover the underlying mutation(s) in its genome that caused the defective colonization phenotype. Eventually Sally and collaborators converged on the answer: the CYCLOPS/IPD3 gene, along with four other genes, had been disrupted in the rmc genotype (Larkan et al., 2007, 2013) to cause the rmc phenotype. The rmc genotype also answered questions about whether a colonised 'nurse' plant can facilitate colonization of a nonmycorrhizal plant (Cavagnaro et al., 2004). This continues to be used to this day as a tool to answer diverse questions relating to AMF function (see Watts-Williams & Cavagnaro, 2014, for a recent review).

Another research topic of Sally's group that was aided by the *rmc* tomato mutant was the intricate work of characterizing AM fungal colonization phenotypes (Pen–, Cort– or Myc+) and morphology (i.e. *Arum* vs *Paris*-type colonization). Due to the disruption of the CYCLOPS/IPD3 gene in *rmc*, colonization by different species of AMF was impaired at different steps in the colonization process, from inability to penetrate the epidermal cells in a few species, up to almost 'normal' functional colonization by one species (Gao *et al.*, 2001). Furthermore, it was discovered with *rmc* that colonization of cortical cells was not an absolute requirement for P or C reciprocal transfer between some AMF species and its host plant (Manjarrez *et al.*, 2008, 2010). Sally's group provided detailed insight into the often overlooked *Paris*-type colonization morphology, concluding that AM morphology is not solely under plant control, but also influenced by fungal identity (species) (Cavagnaro *et al.*, 2001), as well as observing how the *Paris*-type colonization develops and provides P to the host plant (Cavagnaro *et al.*, 2003; also van Arle *et al.*, 2005; Dickson *et al.*, 2007).

Sally produced many papers of the highest possible quality. But more than this, she trained, supported and inspired more people than we can count. For this, we are in her debt.

Stephanie J. Watts-Williams

ID

School of Agriculture, Food & Wine and the Waite Research Institute, The University of Adelaide, Urrbrae, SA 5064, Australia

Timothy R. Cavagnaro

School of Agriculture, Food & Wine and the Waite Research Institute, The University of Adelaide, Urrbrae, SA 5064, Australia

(emails stephanie.watts-williams@adelaide.edu.au (SJW-W); timothy.cavagnaro@adelaide.edu.au (TRC))

References

Barker SJ, Stummer B, Gao L *et al.* 1998. A mutant in *Lycopersicon esculentum* Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation. *The Plant Journal* 15: 791–797.

Baon JB, Smith SE, Alston AM. 1994. phosphorus uptake and growth of barley as affected by soil temperature and mycorrhizal infection. *Journal of Plant Nutrition* 17: 479–492.

Bender SF, Valadares RBdS, Taudiere A. 2014. Mycorrhizas: dynamic and complex networks of power and influence. *New Phytologist* 204: 15–18.

Bruce A, Smith SE, Tester M. 1994. The development of mycorrhizal infection in cucumber: effects of P supply on root growth, formation of entry points and growth of infection units. *New Phytologist* 127: 507–514.

Cavagnaro TR, Gao L, Smith FA. 2001. Morphology of arbuscular mycorrhizas is influenced by fungal identity. *New Phytologist* 151: 469–475.

Cavagnaro TR, Smith FA, Ayling SM, Smith SE. 2003. Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. *New Phytologist* 157: 127–134.

Cavagnaro TR, Smith FA, Hay G, Carne-Cavagnaro VL, Smith SE. 2004a. Inoculum type does not affect overall resistance of an arbuscular mycorrhiza-defective tomato mutant to colonisation but inoculation does change competitive interactions with wild-type tomato. *New Phytologist* 161: 485–494.

Cavagnaro TR, Smith FA, Smith SE. 2004b. Interactions between arbuscular mycorrhizal fungi and a mycorrhiza-defective mutant tomato: does a noninfective fungus alter the ability of an infective fungus to colonise the roots – and vice versa? *New Phytologist* 164: 485–491.

Cavagnaro TR, Smith FA, Smith SE, Jakobsen I. 2005. Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. *Plant, Cell & Environment* 28: 642–650.

Chambers C, Smith SE, Smith FA. 1980. Effects of ammonium and nitrate ions on mycorrhizal infection, nodulation and growth of *Trifolium subterraneum*. *New Phytologist* 85: 47–62.

Dickson S, Smith FA, Smith SE. 2007. Structural differences in arbuscular mycorrhizal symbioses: more than 100 years after Gallaud, where next? *Mycorrhiza* 17: 375–393.

Drew EA, Murray RS, Smith SE. 2006. Functional diversity of external hyphae of AM fungi: ability to colonise new hosts is influenced by fungal species, distance and soil conditions. *Applied Soil Ecology* 32: 350–365.

Ezawa T, Cavagnaro TR, Smith SE *et al.* 2004. Rapid accumulation of polyphosphate in extraradical hyphae of an arbuscular mycorrhizal fungus as revealed by histochemistry and a polyphosphate kinase/luciferase system. *New Phytologist* 161: 387–392.

Ezawa T, Smith SE, Smith FA. 2001a. Differentiation of polyphosphate metabolism between the extra- and intraradical hyphae of arbuscular mycorrhizal fungi. *New Phytologist* 149: 555–563.

Ezawa T, Smith SE, Smith FA. 2001b. Enzyme activity involved in glucose phosphorylation in two arbuscular mycorrhizal fungi: indication that polyP is not the main phosphagen. *Soil Biology & Biochemistry* 33: 1279–1281.

Facelli E, Facelli JM, Smith SE, Mclaughlin MJ. 1999. Interactive effects of arbuscular mycorrhizal symbiosis, intraspecific competition and resource availability on *Trifolium subterraneum* cv. Mt. Barker. *New Phytologist* 141: 535–547.

Gao LL, Delp G, Smith SE. 2001. Colonization patterns in a mycorrhiza-defective mutant tomato vary with different arbuscular-mycorrhizal fungi. *New Phytologist* 151: 477–491.

Geng CN, Zhu YG, Liu WJ, Smith SE. 2005. Arsenate uptake and translocation in seedlings of two genotypes of rice is affected by external phosphate concentrations. *Aquatic Botany* 83: 321–331.

Gianinazzi-Pearson V, Smith SE. 1991. Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. V. Is H¹-ATPase a component of ATP-hydolysing enzyme activities in plant–fungus interfaces? *New Phytologist* 117: 61–74.

Glassop D, Godwin RM, Smith SE, Smith FW. 2007. Rice phosphate transporters associated with phosphate uptake in rice roots colonised with arbuscular mycorrhizal fungi. *Canadian Journal of Botany* 85: 644–651.

Glassop D, Smith SE, Smith FW. 2005. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. *Planta* 222: 688–698.
Grace EJ, Cotsaftis O, Tester M, Smith FA, Smith SE. 2009. Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. *New Phytologist* 181: 938–949.

Harley J, Smith SE. 1983. *Mycorrhizal symbiosis*. Amsterdam, the Netherlands: Academic Press.

Haugen LM, Smith SE. 1992. The effect of high temperature and fallow period on infection of mung bean and cashew roots by the vesicular-arbuscular mycorrhizal fungus *Glomus intraradices*. *Plant and Soil* 145: 71–80.

Jakobsen I, Smith SE, Smith FA, Watts-Williams SJ, Clausen SC, Grønlund M. 2016. Plant growth responses to elevated atmospheric CO₂ are increased by phosphorus sufficiency but not by arbuscular mycorrhizas. *Journal of Experimental Botany* 67: 6173–6186.

Jansa J, Smith FA, Smith SE. 2008. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? *New Phytologist* 177: 779–789.

Lambers H, Ahmedi I, Berkowitz O et al. 2013. Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. *Conservation Physiology* 1: 1–21.

Lambers H, Raven JA, Shaver GR, Smith SE. 2008. Plant nutrient-acquisition strategies change with soil age. *Trends in Ecology and Evolution* 23: 95–103.

Larkan NJ, Ruzicka DR, Edmonds-Tibbett T et al. 2013. The reduced mycorrhizal colonisation (rmc) mutation of tomato disrupts five gene sequences including the CYCLOPS/IPD3 homologue. *Mycorrhiza* 23: 573–584.

Larkan NJ, Smith SE, Barker SJ. 2007. Position of the reduced mycorrhizal colonisation (Rmc) locus on the tomato genome map. *Mycorrhiza* 17: 311–318.

Li HY, Smith FA, Dickson S, Holloway RE, Smith SE. 2008. Plant growth depressions in arbuscular mycorrhizal symbiosis: not just caused by carbon drain? *New Phytologist* 178: 852–862.

Li HY, Smith SE, Holloway RE, Zhu YG, Smith FA. 2006. Arbuscular mycorrhizal (AM) fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. *New Phytologist* 172: 536–543.

Li HY, Zhu YG, Marschner P, Smith FA, Smith SE. 2005. Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. *Plant and Soil* 277: 221–232.

Li HY, Zhu YG, Smith SE, Smith FA. 2003. Phosphorus–zinc interactions in two barley cultivars differing in phosphorus and zinc efficiencies. *Journal of Plant Nutrition* 26: 1085–1099.

Manjarrez M, Christophersen HM, Smith SE, Smith FA. 2010. Cortical colonisation is not an absolute requirement for phosphorus transfer to plants in arbuscular mycorrhizas formed by *Scutellospora calospora* in a tomato mutant: evidence from physiology and gene expression. *Functional Plant Biology* 37: 1132–1142.

Manjarrez M, Smith FA, Marschner P, Smith SE. 2008. Is cortical root colonization required for carbon transfer to arbuscular mycorrhizal fungi? evidence from colonization phenotypes and spore production in the reduced mycorrhizal colonization (RMC) mutant of tomato. *Botany-Botanique* 86: 1009–1019.

Murphy P, Langridge P, Smith SE. 1997. Cloning plant genes differentially expressed during colonization of roots of *Hordeum vulgare* by the vesicular-arbuscular mycorrhizal fungus *Glomus intraradices*. *New Phytologist* 135: 291–301.

Nadian H, Smith SE, Alston A, Murray R. 1996. The effect of soil compaction on growth and P uptake by *Trifolium subterraneum*: interactions with mycorrhizal colonisation. *Plant and Soil* 182: 39–49.

O'Connor PJ, Smith SE, Smith FA. 2002. Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. *New Phytologist* 154: 209–218.

Pattinson G, Smith SE, Doube B. 1997. Earthworm *Aporrectodea trapezoides* had no effect on the dispersal of a vesicular-arbuscular mycorrhizal fungi, *Glomus intraradices*. *Soil Biology and Biochemistry* 29: 1079–1088.

Rosewarne GM, Barker SJ, Smith SE, Smith FA, Schachtman DP. 1999. A *Lycopersicon esculentum* phosphate transporter (*LePTI*) involved in phosphorus uptake from a vesicular-arbuscular mycorrhizal fungus. *New Phytologist* 144: 507–516.

Rosewarne GM, Smith FA, Schachtman DP, Smith SE. 2007. Localization of proton-ATPase genes expressed in arbuscular mycorrhizal tomato plants. *Mycorrhiza* 17: 249–258.

Silsbury J, Smith SE, Oliver A. 1983. A comparison of growth efficiency and specific rate of dark respiration of uninfected and vesicular-arbuscular mycorrhizal plants of *Trifolium subterraneum* L. *New Phytologist* 93: 555–566.

Smith FA, Grace EJ, Smith SE. 2009. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. *New Phytologist* 182: 347–358.

Smith FA, Jakobsen I, Smith SE. 2000. Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with *Medicago truncatula*. *New Phytologist* 147: 357–366.

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Smith SE. 2019. Profile: Sally E. Smith. *New Phytologist* 221: 648–649.

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Smith SE, Dickson S. 1991. Quantification of active vesicular-arbuscular mycorrhizal infection using image analysis and other techniques. *Australian Journal of Plant Physiology* 18: 637–648.

Smith SE, Dickson S, Morris C, Smith FA. 1994. Transfer of phosphate from fungus to plant in VA mycorrhizas: calculation of the area of symbiotic interface and of fluxes of P from two different fungi to *Allium porrum* L. *New Phytologist* 127: 93–99.

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Smith SE, Manjarrez M, Stonor R, McNeill A, Smith FA. 2015. Indigenous arbuscular mycorrhizal (AM) fungi contribute to wheat phosphate uptake in a semi-arid field environment, shown by tracking with radioactive phosphorus. *Applied Soil Ecology* 96: 68–74.

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Stonor RN, Smith SE, Manjarrez M, Facelli E, Smith FA. 2014. Mycorrhizal responses in wheat: shading decreases growth but does not lower the contribution of the fungal phosphate uptake pathway. *Mycorrhiza* 24: 465–472.

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Watts-Williams SJ, Cavagnaro TR. 2014. Nutrient interactions and arbuscular mycorrhizas: a meta-analysis of a mycorrhiza-defective mutant and wild-type tomato genotype pair. *Plant and Soil* 384: 79–92.

Zhu YG, Geng CN, Tong YP, Smith SE, Smith FA. 2006. Phosphate (Pi) and arsenate uptake by two wheat (*Triticum aestivum*) cultivars and their doubled haploid lines. *Annals of Botany* 98: 631–636.

Zhu YG, He YQ, Smith SE, Smith FA. 2002a. Buckwheat (*Fagopyrum esculentum* Moench) has high capacity to take up phosphorus (P) from a calcium (Ca)-bound source. *Plant and Soil* 239: 1.

Zhu YG, Smith FA, Smith SE. 2002b. Phosphorus efficiencies and their effects on Zn, Cu, and Mn nutrition of different barley (*Hordeum vulgare*) cultivars grown in sand culture. *Australian Journal of Agricultural Research* 53: 211–216.

Zhu YG, Smith FA, Smith SE. 2003. Phosphorus efficiencies and responses of barley (*Hordeum vulgare* L.) to arbuscular mycorrhizal fungi grown in highly calcareous soil. *Mycorrhiza* 13: 93–100.

Zhu YG, Smith SE. 2001. Seed phosphorus (P) content affects growth, and P uptake of wheat plants and their association with arbuscular mycorrhizal (AM) fungi. *Plant and Soil* 231: 105–112.

Zhu YG, Smith SE, Barritt AR, Smith FA. 2001a. Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. *Plant and Soil* 237: 249-255.

Zhu YG, Smith SE, Smith FA. 2001b. Plant growth and cation composition of two cultivars of spring wheat (*Triticum aestivum* L.) differing in P uptake efficiency. *Journal of Experimental Botany* 52: 1277–1282.

Zhu YG, Smith SE, Smith FA. 2001c. Zinc (Zn)-phosphorus (P) interactions in two cultivars of spring wheat (*Triticum aestivum* L.) differing in P uptake efficiency. *Annals of Botany* 88: 941–945.

**Key words:** arbuscular mycorrhizal (AM) symbioses, mycorrhizal fungal colonisation, mycorrhizal pathway of P uptake (MPU), Sally E. Smith, Virtual Issue.

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