Plant Science 334 (2023) 111747

Contents lists available at ScienceDirect

Plant Science
journal homepage: www.elsevier.com/locate/plantsci

Review article

The concept of mineral plant nutrient in the light of evolution☆

Guillermo Esteban Santa-María a, *, 1, José Lavres b, 2, Gerardo Rubio c, 3
a
Instituto Tecnológico Chascomús (INTECH), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Universidad Nacional de San Martín
(UNSAM). Escuela de Bio y Nanotecnologías (EByN), UNSAM, Avda. Int. Marino km 8.2. Chascomús, Buenos Aires 7300, Argentina
b
Center for Nuclear Energy in Agriculture (CENA), University of Sao Paulo (USP), Av. Centenário, 303 - São Dimas, CEP: 13416-000 Piracicaba, SP, Brazil
c
Instituto de Investigaciones en Biociencias Agrícolas y Ambientales (INBA), Cátedra de Fertilidad y Fertilizantes, Facultad de Agronomía, Universidad de Buenos Aires,
Av San Martín 4453, Ciudad Autónoma de Buenos Aires, C1417DSE, Argentina

A R T I C L E I N F O A B S T R A C T

Keywords: The concept of mineral plant nutrient has been the subject of a long debate. Here, we suggest that an updated
Beneficial-nutrient discussion on this issue requires considering three dimensions. The first one is ontological as it refers to the
Essential-nutrient fundamentals that underlie the category of being a mineral plant nutrient, the second one refers to the practical
Functional plant element
rules helping to assign a given element to that category, while the third dimension implies the consequences of
Plant evolution
Natural selection
those rules for human activities. We highlight the idea that the definition of what is a mineral plant nutrient can
Sodium be enriched by incorporating an evolutionary perspective, thus giving biological insight and helping to integrate
information from different disciplines. Following this perspective, mineral nutrients can be contemplated as the
elements adopted and/or retained, along evolution, for survival and successful reproduction. We suggest that the
operational rules stated in both early and recent works, while highly valuable for their original purposes, will not
necessarily account for fitness under the conditions prevailing in natural ecosystems where elements were
adopted and are retained -as a result of natural selection processes- covering a wide spectrum of biological ac­
tivities. We outline a new definition that considers the mentioned three dimensions.

1. Introduction
Green photosynthetic plants possess the capacity to grow and survive
on the base of nutrients acquired mainly, or even uniquely, from inor­
ganic sources. The incorporation of these nutrients implies the concerted
activity of shoots and roots, which possess differential anatomical and
functional traits that allow them performing specific nutritional tasks.
Roots, the hidden part of plants, display an exploratory pattern of
growth that permits access to the chemical elements present in soils.
Noticeably, an important amount of the elements in the periodic table
are present in the continental crust although their availability for plants
is highly variable. Given the occurrence of many elements in soils and
the fact that most of them could be eventually found in plants (Reimann
et al., 2001; Kabata-Pendias and Mukherjee, 2007; Watanabe et al.,
2007), major efforts have been made to discern which of these elements
are, at appropriate concentrations, essential, beneficial or without
obvious positive function for plant life. This opens a debate that remains:
what is a mineral plant nutrient?
The criteria for element essentiality have a long history starting from
the seminal works made by von Sachs and Knop in the XIX century.
Those authors proposed the combination of structural and physiological
criteria for the claim of element essentiality (Brown et al., 2022). Briefly,
they were that the element being an integral component of plant sub­
stances and that a given plant cannot complete the vegetation cycle in its
absence. Later on, Arnon and Stout (1939) refined these criteria and
stated three main conditions to be meet for an element be considered as
essential. They are –sometimes with subtle changes- those today
generally accepted: a) a deficiency of the element makes it impossible
for the plant to complete the vegetative or reproductive cycle, b) the
element cannot be replaced by other element (i.e. the deficiency is
specific for the nutrient) and c) the element is directly involved in the
nutrition of the plant. In an influential paper dated on 1994, Emanuel

☆
Dedicated to the memory of Professor Emanuel Epstein (1916–2022)
* Correspondence to: Instituto Tecnológico Chascomús (INTECH), Avda. Int. Marino km 8.2. Chascomús, Buenos Aires 7300, Argentina.
E-mail address: gsantama@intech.gov.ar (G.E. Santa-María).
1
ORCID: 0000-0002-3998-8517
2
ORCID: 0000-0002-7183-4008
3
ORCID: 0000-0001-8419-2473

https://doi.org/10.1016/j.plantsci.2023.111747
Received 4 April 2023; Received in revised form 19 May 2023; Accepted 21 May 2023
Available online 23 May 2023
0168-9452/© 2023 Elsevier B.V. All rights reserved.
G.E. Santa-María et al.
Epstein highlighted the anomalous position of silicon (Si), an element
considered to be essential only for horsetail but that is accumulated by
most plants, in which it plays beneficial roles. It was by further exploring
this element, in a review dated on 1999, when Epstein underscored
major concerns regarding the consistency of the essentiality criteria
above outlined. These insights stimulated a necessary discussion on the
concept of nutrient essentiality that is far from being concluded. In a
recent and interesting paper, Brown et al. (2022) provided a detailed
description of the historical milestones involved in the development of
the concepts of essential and beneficial elements (considering the last
ones as elements that stimulate growth but that do not meet the three
Arnon and Stout criteria). Brown and co-authors have carefully
considered the limitations that surround these concepts and propose a
discussion in terms of plant nutrients instead that in terms of element
essentiality. They advanced the idea that: “A mineral plant nutrient is an
element which is essential or beneficial for plant growth and development or
for the quality attributes of the plant or harvested product, of a given plant
species, grown in its natural or cultivated environment. A plant nutrient may
be considered essential if the life cycle of a diversity of plant species cannot be
completed in the absence of the element. A plant nutrient may be considered
beneficial if it does not meet the criteria of essentiality, but can be shown to
benefit plant growth and development or the quality attributes of a plant or its
harvested product”. It must be noted that this definition cover some
important issues formerly ignored, particularly those relevant for crop
production.
Here we would like to introduce the idea that there are at least three
major dimensions open to debate regarding the concept of mineral plant
nutrient. The first one may be considered ontological as it refers to
which should be the foundations underlying the category of being a
mineral plant nutrient. This perspective may require answering, in
biological terms, the question of what is a mineral nutrient for a living
plant. In this regard, we suggest that the concept of mineral plant
nutrient would gain insight when thought in the light of evolution
considering an ecological context. The second dimension refers to the
operative criteria that would allow researchers to decide whether or not
a given element should be considered as a mineral plant nutrient, i.e.
defining the decision rules that permit –in practical terms- to incorpo­
rate specific elements to the category of being a mineral nutrient. The
third one should contemplate the relevance of these criteria for agri­
cultural practices and human health as illustrated by Brown et al.
(2022). While discussion on the first dimension will impact on our in­
tellectual framework, the third one may influence the public debate and
exert important economic and social consequences. Meanwhile, the
second dimension provides a practical extension for the first one and
could act as a bridge between the other two. We found that previous
definitions focus on the second and/or on the third dimensions, while all
of them –according to their own purposes- leave out the first one. The
purpose of this work more than to provide an exhaustive review on the
mineral nutrient concept is to highlight the relevance and consequences
of incorporating an evolutionary perspective as an adequate basement
for the first dimension. We next examine whether the three dimensions
above outlined may be actually conciliated or if they require the coex­
istence of context-specific definitions. We also argue the convenience to
expand this discussion in terms of functional plant elements instead that
in terms of plant mineral nutrients.
2. The ontological dimension
Theodosius Dobzhansky, the renowned geneticist, entitled his
famous 1973 article with the sentence “Nothing in biology makes sense
except in the light of evolution”. In that article Dobzhansky attempted to
illuminate the central position of evolution as a general system of hy­
pothesis that help to understand life unity and diversity, indicating that
a cumulous of biological facts only acquire a clear meaning in that light.
The biological concept of plant nutrient certainly should not escape from
this key notion as far as the adoption of some elements as nutrients
2
Plant Science 334 (2023) 111747
would be considered the consequence of natural selection processes
positively impacting on the capacity of plants to thrive in their natural
environments. In addition, given the pivotal role of evolution theory,
incorporation of an evolutionary perspective may help to examine the
consistency of the information coming from studies exploring mineral
nutrition from different angles and by different disciplines, thus
providing a unified view on the natural history on mineral plant nutri­
ents. Noticeably, an evolutionary perspective has not been explicitly
discussed and integrated as an intrinsic part of the conceptual frame­
work underlying the mineral plant nutrient concept. Whether or not its
incorporation affects our current ideas deserves to be explored as most
key papers dealing with the concept of mineral plant nutrient do not
contain any clear reference to this matter (e.g. Arnon and Stout, 1939;
Allen and Arnon, 1955; Brown et al., 2022) or just a marginal one
(Bollard and Butler, 1966). Discussions held on that concept have
focused on the search of operational criteria, without specific consid­
eration of their evolutionary bases or their precise correspondence with
them. Even not thoroughly debated, the issue has been not entirely
ignored: in the 1999 review Epstein suggested that Si was evolutionary
adopted as a constituent by plants and in a 2009 article he asked: “What
role has evolution assigned to this element?”. In turn, in a 2003 review,
Subbarao et al. suggested that the essentiality criteria stated by Arnon
and Stout are based on ecological considerations for survival and
reproduction. The idea behind the words of Epstein and Subbarao and
co-workers is that some elements are mineral plant nutrients as a
consequence of the evolution (or ecology) of plants and their pre­
decessors. The involvement of evolution has been further considered for
specific elements, as examined with some detail for selenium (e.g.
White, 2015; Schiavon and Pilon-Smits, 2017). In addition, some au­
thors have explored why certain elements or their compounds have been
evolutionary adopted after considering their physicochemical properties
(e.g. Westheimer, 1987; Williams, 1990). However, none of these au­
thors or other researchers, to our knowledge, attempted to examine the
consequences that the incorporation of an evolutionary perspective may
exert on the concept of mineral nutrient at the whole plant (organismal)
level. In this context, it must be highlighted that some elements of the
periodic table were adopted (and once adopted being retained) as nu­
trients by green photosynthetic organisms or their ancestors as a cor­
ollary of selection directed processes. The consequences that this
evolutionary viewpoint impose on the concept of mineral plant nutrient
need to be examined. It must be noted that exploring the mineral
nutrient concept in the light of evolution makes sense just once
self-replicating entities arose and natural selection began to act (de
Duve, 2005).
As a consequence of the emergence of “omics” and big data science,
along with the developments made in cellular and molecular biology,
new tools are now available to reconstruct some important steps in the
evolution of life, including plants. In this regard, it is thought that an
early endosymbiosis event of a cyanobacteria by a eukaryotic cell gave
origin, between 1 and 1.5 billion years ago, to green algae (Leliaert et al.,
2012). Those early eukaryotic photosynthetic organisms evolved in
aquatic environments from which they obtained the mineral nutrients
required. Land plants (Embriophytes) derive from a specific clade of
these algae (de Vries and Archibald, 2018; Rodrigues et al., 2023). To
our knowledge there are not in-depth studies on the extent to what the
mineral nutrient requirements by the aquatic green plant ancestors
(streptophyte algae) were conserved during the transition to land en­
vironments. Nevertheless, the fact that some elements are used by all
living organisms, suggests a very early adoption consistent with their
role as an intrinsic part of life as we know it. This is an aspect that
involved early prebiotic steps towards the appearance of the proposed
last universal common ancestor (LUCA) and the retention of early
adopted elements in the subsequent history of life (Weiss et al., 2016).
Obvious examples of them, but not unique, are carbon (C), oxygen (O),
hydrogen (H), nitrogen (N), sulphur (S) and phosphorus (P) which play
major structural roles as constituents of macromolecules. Those initial
G.E. Santa-María et al.
adoptions shaped the baseline for the mineral nutrient requirements
later displayed by green algae and higher plants. Clearly, the abundance
as well as the spatial heterogeneity of resources in the terrestrial sub­
strates encountered by first land plants differed from that found by their
ancestors in the aquatic environment. In addition, land plants as sessile
organisms living at the interface among three aggregation states,
differentiate roots and shoots for the acquisition of the resources coming
from below- and above ground. The appearance of key innovations in
body plans, morphology and biochemistry, reciprocally exerted an
important impact on biogeochemical cycles (Morris et al., 2018).
Therefore, during the transition from aquatic to terrestrial environments
as well as during the subsequent coevolution of land plants with the
earth system, plants needed to develop the ability to take up and
distribute mineral nutrients as well as to utilize them for both the basal
and the new emerging functions. We cannot infer, with the current
knowledge, the full picture of gains and losses of mineral plant nutrients
or the precise time point for the emergence or loss of their functions
occurring along plant evolution. As an example of this statement, it was
early proposed that boron assumed a function following land plants
emergence, being its adoption required for the evolution of vascular
plants (Lewis, 1980). However, more recently an interesting debate has
emerged regarding the precise role of this element in plant life, including
the above proposal (Lewis, 2019; 2020; González-Fontes, 2020; Wim­
mer et al., 2020; Pereira et al., 2021). Nevertheless, selected examples
can be given suggesting key steps for the evolutionary functional gain of
certain elements involving either large groups of plants or some
restricted clades. It has been indicated that selenium accumulation arose
repeatedly along evolution (White, 2015; Schiavon and Pilon-Smits,
2017) thus suggesting convergent evolution in a way likely related to
positive selection pressures associated to the benefits conferred by this
element and/or as a byproduct of positive selection for high S accu­
mulation (Schiavon and Pilon-Smits, 2017). A wide survey on the evo­
lution of Si transporters (NIP-III) suggested that selection pressures for Si
uptake may not involve all members of a family, while Si accumulation
show limited variation at the species level (Deshmukh et al., 2020). In
turn, the essential role gained by Na for some plants displaying C4
metabolism (Subbarao et al., 2003) should be associated to the obvious
benefits conferred by that metabolism in certain environments, which
likely evolved independently as this requirement involves members of
different clades. As mentioned by Mayr (1997), the improved use of
environmental resources (mineral ones in the case here considered) can
be favored by selection as it may impact on aspects of the phenotype that
favors survival and/or reproductive success. Mineral plant nutrients, in
this context, can be envisaged as those that were conserved from their
ancestors, or later adopted by a given plant, or group of plant species,
along evolution ensuring the adaptation to a complex and changing
Fig. 1. Some elements present in the earth crust can be adopted and retained
along evolution as functional plant elements. A given element (i.e. orange
circle) may positively impact on pre-existing traits and/or contribute to func­
tional innovations, and subsequently influence survival and/or reproduction,
thus contributing to fitness.
3
Plant Science 334 (2023) 111747
environment (Fig. 1).
If we accept this starting point, the concept of mineral plant nutrient
needs to be rethought in the light of the processes that influence natural
selection, particularly non-random elimination of individuals and se­
lection for reproductive success (Mayr, 1997). Completion of the life
cycle, as required by most essential nutrient definitions, involves sur­
vival while leaves out other key aspects setting fitness1 of plants in their
natural environments which do not seem properly contemplated by the
criteria established by Arnon and Stout. Recently, Kaspari (2021) sug­
gested that the classical laboratory experimental procedures used to test
essentiality according to those criteria may be regarded as a quantifi­
cation of the fundamental niche. However, as also mentioned by this
author, from an ecological perspective we may be more interested in
knowing the impact of nutrients on the realized niche, i.e. the one that
includes the constrains imposed by biotic interactions and environ­
mental fluctuations. It must be noted, given that the Arnon and Stout
criteria involve the completion of the life cycle that they unavoidably
include reproduction as far as no less than a single descendant must be
generated to ensure life cycle completion. However, those criteria per se
do not directly extend towards the reproductive success, at least in terms
of the number of offspring and their later success, which must be
considered of pivotal evolutionary importance. Furthermore, as pointed
out by Subbarao et al. (2003), the Arnon and Stout criteria do not
mandatorily connect with biomass production even though growth –as
we mention in a later section- may be frequently associated with fitness.
All these aspects can be considered for the attempt to advance towards a
plant mineral nutrient notion explicitly based on evolutionary criteria.
1
Here we follow the definition of fitness given by Donovan et al. (2011),
according to which it is the ability of an organism to survive and reproduce,
and thus transmit its genes to the next generation. Fitness is often opera­
tionally defined as the lifetime number of offspring produced.
3. The operative dimension
The approach above outlined may help to provide a conceptual
framework underlying the mineral nutrient concept. However, as stated,
it needs to be companied by operative rules that, certainly, need to be
consistent with the answer offered to what we called the ontological
dimension. Our answer is that some mineral elements once adopted
have been retained along plant evolution, helping to ensure survival and
successful reproduction of plants in both their ancient and contemporary
natural environments. Therefore, the key operative criterion to claim
that a given element is a mineral plant nutrient must be to examine
whether or not fitness (considering the lifetime number of offspring
produced), under the conditions now prevailing in natural ecosystems, is
actually affected by it. A major problem arising from this simple pro­
posal is that fitness cannot be always easily quantified which leads to the
use of proxies. While no universal or unequivocal proxy rule can be
invoked (Orr, 2009; Hendry et al., 2018), it has been argued that the
main performance traits involved in individual plant fitness are vege­
tative biomass, reproductive output (seed biomass plus reproductive
accessories, or seed number) and survival, which in turn are influenced
by morphological, physiological and phenological traits (Violle et al.,
2007). It is by making explicit this rationale that these traits -or their
proxies- may be incorporated as operational criteria to assess if an
element corresponds to the category of plant mineral nutrient based on
evolutionary/ecological criteria. However, the tentative status of the
proxies used need to be emphasized and tested whenever necessary.
From this view any element positively affecting fitness, or their vali­
dated proxies for a given plant in a given environment, can be consid­
ered as a mineral plant nutrient from an operative point of view.
Noticeably this idea does not require to demonstrate that the element
exerts those positive effects in all environments nor than those effects
cannot be substituted by another element. Reciprocally, it does not
require that other plant species (or ecotypes, accessions or even lines),
display similar requirements even in the same environment. In this
G.E. Santa-María et al.
regard, it seems worth mentioning that some mutant lines (either found
in nature or generated in the laboratory) may display different nutri­
tional behavior than their predecessors as suggested by works with the
Lsi1 and Lsi2 rice mutants, which are defective in critical Si transport
processes (Saitoh et al., 2021). Studies with them provided fundamental
genetic evidence for the involvement of Si in key traits determining
plant performance (Ma and Yamaji, 2015).
It is thought that natural selection acts at a phenotypic level. In this
regard, it should be noticed that a fitness-based operative criterion does
not require per se evidence for the specific role played by a given element
in affecting survival and reproduction, as it is the overall phenotypic
performance the one to be evaluated. So, the specific structural,
biochemical or physiological function(s) of mineral plant elements do
not need to be known to support a role for them. This, of course, does not
mean that research on the specific functions of each element should be
abandoned. On the contrary, that research needs to be intensified as it
will offer clarity on the mechanisms by which fitness, or associated
traits, are affected, while also will undoubtedly offer further opportu­
nities for technological interventions. Moreover, studies on these func­
tions, particularly when complemented by consideration of the
physicochemical properties of the elements and the compounds that
they form (Westheimer, 1987; Williams, 1990), may help to understand
why some elements have been adopted. Importantly, knowledge on the
mechanisms affecting fitness will help to discern if the action of a given
element rest on its nutritional capacity and/or as a signal required for
growth and development, being the boundary between these roles less
clear as years go by, as illustrated for potassium (K), N and calcium (Ca)
(Shabala, 2017; Buet et al., 2019; Saito and Uozumi, 2020 and refer­
ences therein). Other functions non related with nourishment or plant
signaling, but equally relevant for plant fitness, can be also envisaged
such as protection against herbivory as shown for Si and Se (Epstein,
1999; Schiavon and Pilon-Smits, 2017; Coskun et al., 2019) and
attraction of pollinators for Na (Finkelstein et al., 2022). In this context,
the use of the third criterion of Arnon and Stout, or some of their variants
(Allen and Arnon, 1955; Epstein, 1965), can be claimed to be valuable to
further distinguish elements able to act in nourishment from those that
may potentially act in other processes. However, a major criticism to this
criterion was raised by Epstein (1999), who observed that it presumes
the existence of adequate knowledge to discern whether or not any
element is directly involved in plant nutrition, thus excluding all the
elements for which no adequate knowledge is available at a given time.
The limits imposed by the use of this third criterion to describe element
functionality have been also critically re-examined in a recent review on
Si (Coskun et al. 2019). Having in mind these criticisms, and considering
that the precise boundaries between nourishment, endogenous signaling
and other relevant functions of mineral elements are not always clear
and may be interactive, it should be considered the convenience to
replace the term “mineral plant nutrient” by the more general concept of
“functional plant element”, thus emphasizing the wide range of func­
tions potentially played by some mineral elements in determining sur­
vival and/or successful reproduction. In order to avoid potential
confusions, here we have kept the use of the term mineral plant nutrient,
but this issue needs to be carefully debated.
Adoption and retention of mineral plant nutrients occurred in nat­
ural environments, where they would impact on different fitness related
traits. In this context, it could be discussed whether or not elements can
be classified according to their effects on survival and reproduction.
While the so called essential nutrients seem to impact on survival and
eventually on traits related with successful reproduction, beneficial el­
ements may be not critical to ensure survival. Nevertheless, the core idea
that an element is essential when its absence leads to impairment at the
vegetative and/or reproductive stage while it cannot be substituted by
another element entirely rest –as formerly mentioned (Epstein, 1999;
Brown et al., 2022)- on the artificial attempt to completely exclude the
given element from a well-known growth media. The origin of that
approach obeyed to the requirement of evaluating the effect of single
4
Plant Science 334 (2023) 111747
elements avoiding the inevitable presence of traces in soils, but also
excluding the indirect effects potentially derived from -and on- the soil
matrix and biotic components, as extensively contemplated by Arnon
(1951). This procedure, in our opinion, had a clear meaning on the base
of a reductionist attitude and led to very important discoveries, but it
does not seem to be consistent with a holistic approach founded on an
evolutionary and ecological point of view if not companied by detailed
studies in real ecosystems. In this regard, it must be highlighted that it
seems extremely unusual that one element being completely absent in
the environment. So, the precise procedures by which we currently show
that survival is affected, by diminishing as far as possible the amount of
the nutrient present in the culture medium, are far away from the con­
ditions prevailing in the ecosystems where plants actually evolved.
Furthermore, as stated by Epstein (1999), those restricting procedures
are largely affected by the limitation of purging elements from experi­
mental cultures. Having in mind these issues, the theoretical difference
between beneficial and essential elements needs to be contrasted with
caution by recognizing the artificial nature of the experiments done to
reveal it and the lack of an adequate ecological context.
4. Towards a holistic view
Most of the work done in mineral nutrition has been performed by
modifying the external concentration of just one or a few elements at a
time. However, both in aquatic and terrestrial ecosystems the adoption
and retention of certain mineral plant nutrients occurred in a medium
containing a complex and highly variable combination of elements in
terms of their abundance. There are important differences among clades
in the accumulation capacity and in the strategies of acquisition
(Watanabe et al., 2007; Rodrigues et al., 2023), being that capacity
strongly influenced by the environment (e.g. Watanabe et al., 2007). The
possibility that the adoption and subsequent retention of an element as a
nutrient could depend, at least partially, on the precise
quali-quantitative combination of the elements offered to plants along
their phylogeny should be seriously considered, particularly bearing in
mind the wide spectrum of physicochemical and biological interactions
existing among elements. In the same way, the existence of present and
past symbiotic and non-symbiotic interactions with the biotic compo­
nents of the environment should be taken into consideration as these
interactions could be key determinants of the nutritional plant perfor­
mance while further impact on growth and other aspects of fitness
(Kaspari, 2020; Hu et al., 2021). Exemplifying this statement, it has been
argued that the ability of plants to symbiotically interact with fungi was
a key trait in early plant colonization (de Vries and Archibald, 2018).
Even restricting the focus to individual plants -leaving aside biotic in­
teractions- it seems important to consider if survival and successful
reproduction, or key traits associated to them, depend either on a single
limiting element or on multiple elements. Let us briefly examine this
issue for growth, which has been considered to be under many cir­
cumstances a useful proxy for plant fitness as it is often positively
associated with fecundity, a key component of leaving viable offspring
(Younginger et al., 2017). According to the “Law of the minimum” early
proposed by C. Sprengel (van der Ploeg et al. 1999), growth at any one
time depends on the scarcest resource, known as the limiting factor (in
our case, a given mineral nutrient). On the contrary, plant growth can be
controlled under a multiple limitation scenario, where several resources
limit it simultaneously. When these alternative possibilities were
examined for Lemma minor (Rubio et al., 2003), it was found that neither
the law of the minimum nor the multiple limitation hypothesis can
explain all plant responses to the major nutrients examined: N, P, K and
magnesium (Mg). In turn, analysis of plant responses to N and P supply
suggest the existence of co-limitation by both nutrients, although the
law of the minimum was considered as a first order approximation
(Ågren et al., 2012). Later studies on aboveground net primary pro­
ductivity performed in grasslands of five continents offered evidence for
the prevalence of the co-limitation hypothesis, while highlighting the
G.E. Santa-María et al.
importance of other elements such as K and micronutrients (Fay et al.,
2015). Therefore, the possibility that co-limitation by resources is a
major driver of some components of fitness should be seriously consid­
ered. If so, in the variable ionic environment actually encountered by
plants along their evolution it was the acquisition and utilization of a
mixture of the available elements which potentially influenced plant
selection processes. This should lead to focus the combinatory effect of
different mineral elements on fitness, or at least in terms of some of its
proxies. As already mentioned the continental crust contains dozens of
chemical elements, being several of them taken up by plants (Reimann
et al., 2001¸ Kabata-Pendias and Mukherjee, 2007). Recent research
indicates that an increasingly number of these elements may impact on
traits potentially related with fitness, particularly in terms of growth, as
exemplified for Titanium (Lyu et al., 2017), Selenium (Schiavon and
Pilon-Smits, 2017) and Iodine (Nascimento et al., 2022), thus adding a
further layer of complexity to the issue. Furthermore, focus on fitness
requires to explore the biotic interactions prevailing in the environment
where plants inhabit and the possible role of mineral elements on them,
as recently explored for cobalt in the context of coevolution of plants and
bacteria (Hu et al., 2021). These interactions may involve multiple
components, and affect multiple processes, as unveiled by extensive soil
microbiome studies (Bahram et al., 2020; Hartmann and Six, 2022).
The complex ionic environment faced by plants as well as the inci­
dence of interactions with other organisms present in the habitat, and
their reciprocal effects on the construction of the niche, opens a debate
on which systems must be used to discern the possible role of a single or
a mixture of elements. Should we explore plant performance and the
ionome in natural ecosystems? should we explore them in greenhouse
soil experiments? or should we perform our studies in culture systems
with defined composition? The answer is that all these approaches must
be used in a complementary way. Experiments varying the doses of
element(s) in soils, or surveys conveying different environments, could
help to assess possible effects on fitness, including those derived from
interactions with biotic components or derived from lab non-
reproducible soil properties. In turn, culture in well-defined media,
such as the commonly used hydroponic systems, may help to discern the
role of individual -or a mix of- element(s) for plants in setting plant
fitness components and to explore the physiological, biochemical and
molecular mechanisms involved. Certainly, the extrapolation from one
to another system should be done with caution, as key processes acting
in ecosystems may be not properly mimicked in controlled media and
reciprocally work at the ecosystem level may confuse the actual rele­
vance of specific elements on individual plants. An integrative approach
based on collaborative efforts by plant physiologists, soil scientists and
ecologists is, beyond any doubt, fruitful.
5. Sodium as a mineral nutrient for plants
Let us briefly examine the issues mentioned for the element Na. This
element shares extensive physicochemical attributes with K. However,
while K has been early recognized as an essential element for living
organisms, including plants, Na is -for most plants- not considered an
essential element according to the strict Arnon and Stout criteria. In fact,
Na is considered essential only for a limited subset of plants displaying
C4 metabolism. Nevertheless, several researchers have pointed out the
relevance of Na in plant life –including C3 plants- as well as its major
impact on the structure and function of ecosystems (Subbarao et al.,
2003; Kaspari, 2020), being proposed to consider it as a functional plant
nutrient (Subbarao et al. 2003). In turn, the roles -and the mechanisms
for the control- of K and Na nutrition along life evolution, particularly
those referred to green photosynthetic organisms, have been dissected
from different perspectives (e.g. Benito et al., 2014; Britto et al., 2021).
As described by these authors early marine cells tended to accumulate K
and exclude Na, which allowed –for organisms thriving in marine en­
vironments- the energization of the plasma membrane (Benito et al.,
2014; Britto et al., 2021). The change from a “sodium economy” towards
5
Plant Science 334 (2023) 111747
a “proton economy” occurring during the transition from marine to land
freshwaters and soils, leaded to the prevalence in plants and other or­
ganisms of a differential array of transport entities, coupled to energi­
zation through a ΔH+ gradient generated by H+-ATPases, being possible
the coexistence of both economies in some transitional forms. Likely this
nutritional transition constituted a critical step in the colonization (and
the subsequent modification) of the earth landscape. Noticeably, Na and
K are widespread in the continental crust being there highly abundant
elements. The availability of these elements, of course, is not uniform
among different types of soils as well as in aquatic environments, thus
opening the possibility that selection pressures for the acquisition and
exclusion of Na may be highly variable across environments, being the
mechanisms involved in the underlying transport processes studied in
detail in the context of salt resistance (Yamaguchi and Blumwald, 2005;
Benito et al., 2014). Noticeably, just some functions played by K appear
to be highly specific. Therefore, in low K-availability environments, Na
can partially substitute for K as studied in different plant species (e.g.
Hartley et al., 2020; Battie-Laclau et al., 2013; Mateus et al., 2021) being
this conceivably a universal pattern, likely affecting the critical con­
centration of K at which maximum growth is achieved while helping to
maintain cell turgor. Under low K conditions, very large differences in
the capacity to accumulate Na have been observed even within a given
species (e.g. Moriconi et al., 2022). The appearance of large differences
in Na accumulation has been historically connected with differential
resistance to some forms of salinity but it could be, in an inverse way,
connected with differential performance under low K environments. In
addition to the well-known beneficial effects of adequate Na availability
for plants dwelling in low K environments, Na has been also shown to
benefit plant growth in a way not directly related to functional K
replacement. Some species showed beneficial effects of Na on growth
even under conditions of adequate K supply (Subbarao et al., 2003).
The positive effects of low Na accumulation on plant fitness just
mentioned, refer to survival (for some C4 plants), enhanced growth at
adequate K supplies for some species, and improved performance in low
K environments for likely all plant species. They, certainly, could pro­
vide a good argument for the claim that Na is a mineral plant nutrient
adopted during plant evolution as far as it may improve plant perfor­
mance according to at least one, or two of the fitness proxies above
outlined. However, it seems worth to note that in an ecological context
this element may further impact the relationship between plants and
other components of the biota. For example, as pointed out by Kaspari
(2020), it seems possible that plants along their evolution manipulated
Na accumulation to enhance or diminish the appeal for consumers,
which may indicate the existence of selection pressures driven by the
biota to modulate Na capture and distribution within plants. Particu­
larly, the attraction of consumers will eventually impose a cost that need
to be counterbalanced by benefits on plant fitness. In this regard, a
recent work has shown that enhancing Na accumulation in nectar en­
hances the diversity as well as the frequency of visiting pollinators for
which Na is considered a key nutrient (Finkelstein et al., 2022) thus
potentially influencing plant reproductive success by affecting a key
process contributing to the offspring number. This kind of effects are
clearly beyond the scope of the Arnon and Stout criteria, as well as from
the controlled growth procedures commonly used, as they operate in an
ecological context. However, they are undoubtedly relevant from a
fitness perspective.
The claim that plants evolved in variable Na environments and that
use this element to improve plant performance needs to be further
connected with its nutrition. It could be expected that if land plants
adopted or retained Na as a functional element, they possess transport
systems specifically devoted to mediate Na transport into cells, partic­
ularly from low Na concentrations, and that these systems were devel­
oped or conserved along plant evolution. In this regard, it was
unexpectedly recognized almost 30 years ago that plants actually
possess a family of transport systems (HKTs) whose major roles are to
mediate inward Na fluxes even from very diluted external Na
G.E. Santa-María et al.
concentrations either alone or coupled with K transport (Rubio et al.,
1995; Benito et al., 2014). Similarly, it has been also shown even with a
lesser degree of characterization, that the largest known family of plant
K transporters (KT-HAK-KUP) contains a clade (IV), originated early
during the transition from aquatic to terrestrial environments (Santa-­
María et al., 2018), whose members up to now characterized have the
capacity to mediate Na transport from diluted Na solutions (Benito et al.,
2012; Zhang et al., 2019; Wang et al., 2020). While some HKT and Clade
IV KT-HAK-KUP transporters play a major role in plant acclimation to
salinity, affecting long distance Na transport (Ali et al., 2021; Zhang
et al., 2019; Wang et al., 2020), other members of these groups are
known to be involved in Na transport from the external medium under
conditions of low K availability (Ali et al., 2021; Benito et al., 2012). In
turn, members of the CCC family of transporters (Colmenero-Flores
et al., 2007), conserved during the evolution of land plants, have been
debated as key determinants of the long-distance movement of this
element (Zhu et al., 2017; Henderson et al., 2018). It should be also
mentioned the proposal that, under some environmental conditions,
xylem loading of Na can be a thermodynamically uphill process (Sha­
bala, 2013), which implies energy expenditure in a key process of Na
transport. All these observations suggest that the evolution of Na
transport systems in plants was a process driven by selection pressures
favoring the use of Na, a widespread resource involved in plant survival
and/or reproduction.
6. Towards an integrated definition
At the onset of this article we mentioned three dimensions to be
tackled, being the third one referred to the need of a definition
compatible with agricultural practices. Brown et al. (2022) offered
compelling arguments to support this need, and the reader is referred
there for a full discussion. In this regard, it must be mentioned that se­
lection pressures acting on plants in wild environments do not neces­
sarily work in the same direction that human directed selection, which is
oriented towards the quanti-qualitative maximization of traits desirable
for social and economic purposes. Human directed selection involves
both classical and modern-molecular breeding methods that can
generate genetically modified plants, even in a short period of time.
Although human directed evolution could be considered an integral part
of the evolution of life, emerging traits raised by current technologies
have not necessarily faced the selection filters operating in natural en­
vironments. Therefore, these traits may not contribute per se to fitness in
natural ecosystems where plants evolved over millions of years and
where likely more than 450000 living plant species thrive (Pimm and
Raven, 2017). Reciprocally, traits relevant for plant fitness in natural
environments (as the accumulation of some elements in fruits) can be
detrimental for human purposes. Therefore, a possible divergence be­
tween the legacy of pre-agricultural evolution with our human goals
may be occasionally present, affecting in some cases key nutritional
traits (Ford Denisson and Kiers, 2005). Consequently, it should be not
expected to reach a perfect conciliation between a mineral plant nutrient
concept based -as proposed here- on evolutionary/ecological founda­
tions with a definition focused on the public responsibility of research in
plant nutrition. Having in mind these conflicts, we suggest that the
ontological aspect firstly mentioned, which may confer biological
insight to the definition of mineral plant nutrient particularly consid­
ering an ecological context, should be distinguished from the agricul­
tural needs. That distinction, once recognized, could be part of a
definition that takes into consideration all the necessary perspectives. In
this regard, we propose to distinguish the evolutionary/ecological
viewpoint from the agricultural one.
Based on the above background, we advance the following defini­
tion: “from a biological point of view, mineral plant nutrients are the elements
that were conserved from their ancestors, or later adopted, by a given plant or
group of plant species along their evolution to favor their adaptation, in terms
of survival and/or successful reproduction in their natural environments.
6
Plant Science 334 (2023) 111747
According to the components of fitness affected, plant nutrients can be
theoretically grouped into essentials, those needed for the completion of the
life cycle, or beneficial, those that only impact on other aspects of fitness.
From an agricultural point of view, as indicated by Brown et al. (2022), a
mineral plant nutrient is an element which is essential or beneficial for plant
growth and development or for the quality attributes of the plant or harvested
product, of a given plant species.”
7. Concluding remarks
In this manuscript we attempted to highlight an aspect that was not
explicitly addressed in previous discussions on the definitions of mineral
plant nutrients. In our view, fruitful discussions should consider an
evolutionary perspective in order to reach a concept with a wide bio­
logical meaning that considers the complex relationships between plants
and biotic and abiotic components. In turn, an evolutionary point of
view lead to consider fitness, in terms of survival and successful repro­
duction, as the key attribute for the adoption and retention of elements
for functional roles. While several proxies of fitness can be used for
operative assignation of an element to the category of being a functional
plant element, they need to be validated in natural environments.
Certainly, some of those proxies, particularly those related with biomass
accumulation and development, can be well suited when considering
fitness for agricultural purposes. The incorporation of the evolutionary
perspective, along with the introduction of the functional plant element
term, may endow increased plasticity to this concept allowing to provide
a global and integrated picture on how plants incorporate and utilize the
captured elements for a broad spectrum of biological functions. In
addition, this debate may be interesting, when based on the joined ef­
forts of physiologists, ecologists, agronomists as well as researchers
formed in other disciplines, to integrate this concept within the widely
discussed theoretical corpus of evolutionary biology.
Funding
This work was supported by the PICT-2019-03103 to G.E.S-M. JL is
grateful to CNPq for the productivity grant # 310572/2017-7. G.E.S-M
and G.R thanks Consejo Nacional de Investigaciones Científicas y
Técnicas.
CRediT authorship contribution statement
GES-M led the project and wrote the initial draft. GES-M, JL and GR
contributed to the conception of the work, manuscript writing and
editing. The three authors approved the final version.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data Availability
No data was used for the research described in the article.
Acknowledgements
The authors would like to express gratitude to Professor Begoña
Benito (Universidad Politécnica de Madrid, Madrid, Spain) for critical
reading of an early version of this manuscript. Thanks are also given to
Professor Jorge Dubcovsky (University of California, Davis, USA) for
help with bibliography. We also thanks to the many colleagues that
along many decades contributed to decipher the roles of plant mineral
nutrients: we apologize for being not able to cite all their key contri­
butions. We also thank the anonymous reviewers for their valuable
G.E. Santa-María et al.
suggestions that helped to improve the manuscript.
References
G.I. Ågren, J.Å.M. Wetterstedt, M.F.K. Billberger, Nutrient limitation on terrestrial plant
growth – modeling the interaction between nitrogen and phosphorus, N. Phytol. 194
(2012) 953–960, https://doi.org/10.1111/j.1469-8137.2012.04116.x.
A. Ali, N. Raddatz, J.M. Pardo, D.-J. Yun, HKT sodium and potassium transporters in
Arabidopsis thaliana and related halophyte species, Physiol. Plant. 171 (2021)
546–558, https://doi.org/10.1111/ppl.13166.
M.B. Allen, D.I. Arnon, Studies on nitrogen-fixing blue-green algae. II. The sodium
requirement of Anabaena cylindrica, Physiol. Plant 8 (1955) 653–660, https://doi.
org/10.1111/j.1399-3054.1955.tb07758.x.
D.I. Arnon, Growth and function as criteria in determining the essential nature of
inorganic nutrients, in: E. Truog (Ed.), Mineral Nutrition Of Plants, University of
Wisconsin Press, Madison, 1951, pp. 313–341.
D.I. Arnon, P.R. Stout, The essentiality of certain elements in minute quantity for plants
with special reference to copper, Plant Physiol. 14 (1939) 371–375, https://doi.org/
10.1104/pp.14.2.371.
M. Bahram, T. Netherway, F. Hildebrand, K. Pritsch, R. Drenkhan, K. Loit, S. Anslan,
P. Bork, L. Tedersoo, Plant nutrient-acquisition strategies drive topsoil microbiome
structure and function, N. Phytol. 227 (2020) 1189–1199, https://doi.org/10.1111/
nph.16598.
P. Battie-Laclau, J.-P. Laclau, M. de, C. Piccolo, B.C. Arenque, C. Beri, L. Mietton, M.R.
A. Muniz, L. Jordan-Meille, M.S. Buckeridge, Y. Nouvellon, J. Ranger, J.-P. Bouillet,
Influence of potassium and sodium nutrition on leaf area components in Eucalyptus
grandis trees, Plant Soil 371 (2013) 19–35, https://doi.org/10.1007/s11104-013-
1663-7.
B. Benito, B. Garciadeblas, A. Rodriguez-Navarro, HAK transporters from Physcomitrella
patens and Yarrowia lipolytica mediate sodium uptake, Plant Cell Physiol. 53 (2012)
1117–1123, https://doi.org/10.1093/pcp/pcs056.
B. Benito, R. Haro, A. Amtmann, T.A. Cuin, I. Dreyer, The twins K+ and Na+ in plants,
J. Plant Physiol. 171 (2014) 723–731, https://doi.org/10.1016/j.jplph.2013.10.014.
E.G. Bollard, G.W. Butler, Mineral nutrition of plants, Annu. Rev. Plant. Physiol. 17
(1966) 77–112, https://doi.org/10.1146/annurev.pp.17.060166.000453.
D.T. Britto, D. Coskun, H.J. Kronzucker, Potassium physiology from archean to holocene:
a higher-plant perspective, J. Plant Physiol. 262 (2021), 153432, https://doi.org/
10.1016/j.jplph.2021.153432.
P.H. Brown, F.-J. Zhao, A. Dobermann, What is a plant nutrient? Changing definitions to
advance science and innovation in plant nutrition, Plant Soil 476 (2022) 11–23,
https://doi.org/10.1007/s11104-021-05171-w.
A. Buet, A. Galatro, F. Ramos-Artuso, M. Simontacchi, Nitric oxide and plant mineral
nutrition: current knowledge, J. Exp. Bot. 70 (2019) 4461–4476, https://doi.org/
10.1093/jxb/erz129.
J.M. Colmenero-Flores, G. Martínez, G. Gamba, N. Vázquez, D.J. Iglesias, J. Brumós,
M. Talón, Identification and functional characterization of cation–chloride
cotransporters in plants, 278-192, Plant J. 50 (2007), https://doi.org/10.1111/
j.1365-313X.2007.03048.x.
D. Coskun, R. Deshmukh, H. Sonah, J.G. Menzies, O. Reynolds, J.F. Ma, H.J. Kronzucker,
R.R. Bélanger, The controversies of silicon’s role in plant biology, N. Phytol. 221
(2019) 67–85, https://doi.org/10.1111/nph.15343.
R.R. van der Ploeg, W. Böhm, M.B. Kirkham, On the origin of the theory of mineral
nutrition of plants and the law of the minimum, Soil Sci. Soc. Am. J. 63 (1999)
1055–1062.
R. Deshmukh, H. Sonah, R.R. Belanger, New evidence defining the evolutionary path of
aquaporins regulating silicon uptake in land plants, J. Exp. Bot. 71 (2020)
6775–6788, https://doi.org/10.1093/jxb/eraa342.
T. Dobzhansky, Nothing in biology makes sense except in the light of evolution, Am. Biol.
Teach. 35 (1973) 125–129, https://doi.org/10.2307/4444260.
L.A. Donovan, H. Maherali, C.M. Caruso, H. Huber, H. de Kroon, The evolution of the
worldwide leaf economics spectrum, Trends Ecol. Evol. 26 (2011) 88–95, https://
doi.org/10.1016/j.tree.2010.11.011.
C. de Duve, The onset of selection, Nature 433 (2005) 581–582, https://doi.org/
10.1038/433581a.
E. Epstein, Mineral metabolism, in: J. Bonner, J.E. Varner (Eds.), Plant Biochemistry,
Elsevier, Amsterdam, 1965, pp. 438–466.
E. Epstein, The anomaly of silicon in plant biology, Proc. Natl. Acad. Sci. USA 91 (1994)
11–17, https://doi.org/10.1073/pnas.91.1.11.
E. Epstein, Silicon, Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 50 (1999) 641–664,
https://doi.org/10.1146/annurev.arplant.50.1.641.
E. Epstein, Silicon: its manifold roles in plants, Ann. Appl. Biol. 155 (2009) 155–160,
https://doi.org/10.1111/j.1744-7348.2009.00343.x.
P.A. Fay, S.M. Prober, W.S. Harpole, J.M.H. Knops, J.D. Bakker, E.T. Borer, E.M. Lind, A.
S. MacDougall, E.W. Seabloom, P.D. Wragg, P.B. Adler, D.M. Blumenthal, Y.
M. Buckley, C. Chu, E.E. Cleland, S.L. Collins, K.F. Davies, G. Du, X. Feng, J. Firn, D.
S. Gruner, N. Hagenah, Y. Hautier, R.W. Heckman, V.L. Jin, K.P. Kirkman, J. Klein, L.
M. Ladwig, Q. Li, R.L. McCulley, B.A. Melbourne, C.E. Mitchell, J.L. Moore, J.
W. Morgan, A.C. Risch, M. Schütz, C.J. Stevens, D.A. Wedin, L.H. Yang, Grassland
productivity limited by multiple nutrients, Nat. Plants 1 (2015) 15080, https://doi.
org/10.1038/nplants.2015.80.
C.J. Finkelstein, P.J. CaraDonna, A. Gruver, E.A.R. Welti, M. Kaspari, N.J. Sanders,
Sodium-enriched floral nectar increases pollinator visitation rate and diversity, Biol.
Lett. 18 (2022) 20220016, https://doi.org/10.1098/rsbl.2022.0016.
7
Plant Science 334 (2023) 111747
R. Ford Denisson, T. Kiers, Sustainable crop nutrition: constraints and opportunities, in:
M. Broadley, P.J. White (Eds.), Plant Nutritional Genomics, Blackwell Publishing,
Oxford (UK), 2005, pp. 242–286.
A. González-Fontes, Why boron is an essential element for vascular plants: a comment on
Lewis (2019) ‘Boron: the essential element for vascular plants that never was,
N. Phytol. 226 (2020) 1228–1230, https://doi.org/10.1111/nph.16033.
T.N. Hartley, A.S. Thomas, F.J.M. Maathuis, A role for the OsHKT2;1 sodium transporter
in potassium use efficiency in rice, J. Exp. Bot. 71 (2020) 699–706, https://doi.org/
10.1093/jxb/erz113.
M. Hartmann, J. Six, Soil structure and microbiome functions in agroecosystems, Nat.
Rev. Earth Environ. 4 (2022) 4–18, https://doi.org/10.1038/s43017-022-00366-w.
S. Henderson, S. Wege, M. Gilliham, Plant cation-chloride cotransporters (CCC):
evolutionary origins and functional insights, Int. J. Mol. Sci. 19 (2018) 492, https://
doi.org/10.3390/ijms19020492.
A.P. Hendry, D.J. Schoen, M.E. Wolak, J.M. Reid, The contemporary evolution of fitness,
Annu. Rev. Ecol. Evol. Syst. 49 (2018) 457–476, https://doi.org/10.1146/annurev-
ecolsys-110617-062358.
X. Hu, X. Wei, J. Ling, J. Chen, Cobalt: an essential micronutrient for plant growth, Front.
Plant Sci. 12 (2021), 768523, https://doi.org/10.3389/fpls.2021.768523.
A. Kabata-Pendias, A.B. Mukherjee, Trace Elements from Soil to Human, Springer Berlin
Heidelberg, Berlin, Heidelberg, 2007, https://doi.org/10.1007/978-3-540-32714-1.
M. Kaspari, The seventh macronutrient: how sodium shortfall ramifies through
populations, food webs and ecosystems, Ecol. Lett. 23 (2020) 1153–1168, https://
doi.org/10.1111/ele.13517.
M. Kaspari, The invisible hand of the periodic table: how micronutrients shape ecology,
Annu. Rev. Ecol. Evol. Syst. 52 (2021) 199–219, https://doi.org/10.1146/annurev-
ecolsys-012021-090118.
F. Leliaert, D.R. Smith, H. Moreau, M.D. Herron, H. Verbruggen, C.F. Delwiche, O. De
Clerck, Phylogeny and molecular evolution of the green algae, Crit. Rev. Plant Sci.
31 (2012) 1–46, https://doi.org/10.1080/07352689.2011.615705.
D.H. Lewis, Boron, lignification and the origin of vascular plants-a unified hypothesis,
N. Phytol. 84 (1980) 209–229, https://doi.org/10.1111/j.1469-8137.1980.tb04423.
x.
D.H. Lewis, Boron: the essential element for vascular plants that never was, N. Phytol.
221 (2019) 1685–1690, https://doi.org/10.1111/nph.15519.
D.H. Lewis, The status of boron as an essential element for vascular plants: II. A response
to Wimmer et al. (2020) ‘Boron: an essential element for vascular plants, N Phytol.
226 (2020) 1238–1239, https://doi.org/10.1111/nph.16128.
S. Lyu, X. Wei, J. Chen, C. Wang, X. Wang, D. Pan, Titanium as a beneficial element for
crop production, Front. Plant Sci. 8 (2017) 597, https://doi.org/10.3389/
fpls.2017.00597.
J.F. Ma, N. Yamaji, A cooperative system of silicon transport in plants, Trends Plant Sci.
20 (2015) 435–442, https://doi.org/10.1016/j.tplants.2015.04.007.
N.S. Mateus, A.L. Florentino, E.F. Santos, A. de, V. Ferraz, J.L. de, M. Goncalves,
J. Lavres, Partial substitution of K by Na alleviates drought stress and increases water
use efficiency in Eucalyptus Species seedlings, Front. Plant Sci. 12 (2021) 632342,
https://doi.org/10.3389/fpls.2021.632342.
E. Mayr, The objects of selection, Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 2091–2094,
https://doi.org/10.1073/pnas.94.6.2091.
J.I. Moriconi, M. Silva, J. Zhang, G.E. Tranquilli, G.E. Santa-María, A genome-wide
association study unveils key chromosome regions involved in determining sodium
accumulation in wheat under conditions of low potassium supply, J. Plant Physiol.
275 (2022), 153739, https://doi.org/10.1016/j.jplph.2022.153739.
J.L. Morris, M.N. Puttick, J.W. Clark, D. Edwards, P. Kenrick, S. Pressel, C.H. Wellman,
Z. Yang, H. Schneider, P.C.J. Donoghue, The timescale of early land plant evolution,
Proc. Natl. Acad. Sci. USA 115 (2018), https://doi.org/10.1073/pnas.1719588115.
V.L. Nascimento, B.C.O.Q. Souza, G. Lopes, L.R.G. Guilherme, On the role of iodine in
plants: a commentary on benefits of this element, Front. Plant Sci. 13 (2022),
836835, https://doi.org/10.3389/fpls.2022.836835.
H.A. Orr, Fitness and its role in evolutionary genetics, Nat. Rev. Genet. 10 (2009)
531–539, https://doi.org/10.1038/nrg2603.
G.L. Pereira, J.A. Siqueira, W. Batista-Silva, F.B. Cardoso, A. Nunes-Nesi, W.L. Araújo,
Boron: more than an essential element for land plants? Front. Plant Sci. 11 (2021),
610307 https://doi.org/10.3389/fpls.2020.610307.
S.L. Pimm, P.H. Raven, The fate of the world’s plants, Trends Ecol. Evol. 32 (2017)
317–320, https://doi.org/10.1016/j.tree.2017.02.014.
C. Reimann, F. Koller, B. Frengstad, G. Kashulina, H. Niskavaara, P. Englmaier,
Comparison of the element composition in several plant species and their substrate
from a 1 500 000-km2 area in Northern Europe, Sci. Total Environ. 278 (2001)
87–112, https://doi.org/10.1016/S0048-9697(00)00890-1.
W.F.C. Rodrigues, A.B.P. Lisboa, J.E. Lima, F.K. Ricachenevsky, L. Del-Bem, Ferrous iron
uptake via IRT1/ZIP evolved at least twice in green plants, N. Phytol. 237 (2023)
1951–1961, https://doi.org/10.1111/nph.18661.
F. Rubio, W. Gassmann, J.I. Schroeder, Sodium-driven potassium uptake by the plant
potassium transporter HKT1 and mutations conferring salt tolerance, Science 270
(1995) 1660–1663, https://doi.org/10.1126/science.270.5242.1660.
G. Rubio, J. Zhu, J.P. Lynch, A critical test of the two prevailing theories of plant
response to nutrient availability, Am. J. Bot. 90 (2003) 143–152, https://doi.org/
10.3732/ajb.90.1.143.
S. Saito, N. Uozumi, Calcium-regulated phosphorylation systems controlling uptake and
balance of plant nutrients, Front. Plant Sci. 11 (2020) 44, https://doi.org/10.3389/
fpls.2020.00044.
Y. Saitoh, N. Mitani-Ueno, K. Saito, K. Matsuki, S. Huang, L. Yang, N. Yamaji, H. Ishikita,
J.-R. Shen, J.F. Ma, M. Suga, Structural basis for high selectivity of a rice silicon
channel Lsi1, Nat. Commun. 12 (2021) 6236, https://doi.org/10.1038/s41467-021-
26535-x.
G.E. Santa-María et al.
G.E. Santa-María, S. Oliferuk, J.I. Moriconi, KT-HAK-KUP transporters in major
terrestrial photosynthetic organisms: a twenty years tale, J. Plant Physiol. 226
(2018) 77–90, https://doi.org/10.1016/j.jplph.2018.04.008.
M. Schiavon, E.A.H. Pilon-Smits, The fascinating facets of plant selenium accumulation –
biochemistry, physiology, evolution and ecology, N. Phytol. 213 (2017) 1582–1596,
https://doi.org/10.1111/nph.14378.
S. Shabala, Learning from halophytes: physiological basis and strategies to improve
abiotic stress tolerance in crop, Ann. Bot. 112 (2013) 1209–1221, https://doi.org/
10.1093/aob/mct205.
S. Shabala, Signalling by potassium: another second messenger to add to the list? J. Exp.
Bot. 68 (2017) 4003–4007, https://doi.org/10.1093/jxb/erx238.
G.V. Subbarao, O. Ito, W.L. Berry, R.M. Wheeler, Sodium-a functional plant nutrient,
Crit. Rev. Plant Sci. 22 (2003) 391–416, https://doi.org/10.1080/
07352680390243495.
C. Violle, M.-L. Navas, D. Vile, E. Kazakou, C. Fortunel, I. Hummel, E. Garnier, Let the
concept of trait be functional!, Oikos 116 (2007) 882–892, https://doi.org/10.1111/
j.0030-1299.2007.15559.x.
J. de Vries, J.M. Archibald, Plant evolution: landmarks on the path to terrestrial life,
N. Phytol. 217 (2018) 1428–1434, https://doi.org/10.1111/nph.14975.
Z. Wang, Y. Hong, G. Zhu, Y. Li, Q. Niu, J. Yao, K. Hua, J. Bai, Y. Zhu, H. Shi, S. Huang,
J. Zhu, Loss of salt tolerance during tomato domestication conferred by variation in a
Na + /K + transporter, EMBO J. 39 (2020), https://doi.org/10.15252/
embj.2019103256.
T. Watanabe, M.R. Broadley, S. Jansen, P.J. White, J. Takada, K. Satake, T. Takamatsu, S.
J. Tuah, M. Osaki, Evolutionary control of leaf element composition in plants,
N. Phytol. 174 (2007) 516–523, https://doi.org/10.1111/j.1469-8137.2007.02078.
x.
Plant Science 334 (2023) 111747
M.C. Weiss, F.L. Sousa, N. Mrnjavac, S. Neukirchen, M. Roettger, S. Nelson-Sathi, W.
F. Martin, The physiology and habitat of the last universal common ancestor, Nat.
Microbiol 1 (2016) 16116, https://doi.org/10.1038/nmicrobiol.2016.116.
F.H. Westheimer, Why nature chose phosphates, Science 235 (1987) 1173–1178,
https://doi.org/10.1126/science.2434996.
P.J. White, Selenium accumulation by plants, Ann. Bot. (2015) mcv180, https://doi.org/
10.1093/aob/mcv180.
R.J.P. Williams, Bio-inorganic chemistry: its conceptual evolution, Coord. Chem. Rev.
100 (1990) 573–610, https://doi.org/10.1016/0010-8545(90)85020-S.
M.A. Wimmer, I. Abreu, R.W. Bell, M.D. Bienert, P.H. Brown, B. Dell, T. Fujiwara, H.
E. Goldbach, T. Lehto, H. Mock, N. Wirén, E. Bassil, G.P. Bienert, Boron: an essential
element for vascular plants: A comment on Lewis, 2019. ‘Boron: the essential
element for vascular plants that never was, N. Phytol. 226 (2020) 1232–1237,
https://doi.org/10.1111/nph.16127.
T. Yamaguchi, E. Blumwald, Developing salt-tolerant crop plants: challenges and
opportunities, Trends Plant Sci. 10 (2005) 615–620, https://doi.org/10.1016/j.
tplants.2005.10.002.
B.S. Younginger, D. Sirová, M.B. Cruzan, D.J. Ballhorn, Is biomass a reliable estimate of
plant fitness? Appl. Plant Sci. 5 (2017) 1600094, https://doi.org/10.3732/
apps.1600094.
M. Zhang, X. Liang, L. Wang, Y. Cao, W. Song, J. Shi, J. Lai, C. Jiang, A HAK family Na+
transporter confers natural variation of salt tolerance in maize, Nat. Plants (2019)
1297–1308, https://doi.org/10.1038/s41477-019-0565-y.
M. Zhu, M. Zhou, L. Shabala, S. Shabala, Physiological and molecular mechanisms
mediating xylem Na+ loading in barley in the context of salinity stress tolerance,
Plant Cell Environ. 40 (2017) 1009–1020, https://doi.org/10.1111/pce.12727.