https://live.childrenshealthdefense.org/chd-tv/shows/good-morning-chd/from-volcanoes-to-vitality-natures-mineral-code/

A reader sent the following article, which supports many of Pierre’s contentions. Because Substack has stopped allowing pdf’s, I am forced to present it in the following unsatisfactory format.

Or go here to download the full pdf.

https://link.springer.com/article/10.1007/s11104-021-05171-w

Vol.:(0123456789)

1 3

Plant Soil

https://doi.org/10.1007/s11104-021-05171-w

SPECIAL ISSUE S97 – 30 YEARS

What is a plant nutrient? Changing definitions to advance

science and innovation in plant nutrition

Patrick H. Brown . Fang‑Jie Zhao .

Achim Dobermann

Received: 9 July 2021 / Accepted: 27 September 2021

© The Author(s) 2021

tolerance or pest and disease resistance. We propose

an open scientific debate to refine and implement this

updated definition of plant nutrients. Other outcomes

of this debate could be a more precise definition of

the experimental evidence required to classify an element

as a plant nutrient, and an independent scientific

body to regularly review the list of essential and

beneficial nutrients. The debate could also attempt to

refine the definition of plant nutrients to better align

with nutrients deemed essential for animal and human

nutrition, thus following a more holistic ’one nutrition‘

concept.

Keywords Plant nutrients · Definition · Essential

elements · Beneficial elements

A new paradigm for plant nutrition

Plant scientists as well as regulatory bodies largely

adhere to a rigid definition of essential mineral elements

(or nutrients) for plants that was originally proposed

in 1939 (Arnon and Stout 1939), and has been

repeated in standard monographs on plant nutrition

ever since. This very narrow definition of essentiality

considers an element as a plant nutrient only in the

context of the completion of the lifecycle of the plant.

It excludes from consideration many plant nutrients

that ‘only’ enhance plant growth, improve the efficiency

of utilization of nutrients, water, and other

resources, enhance abiotic or biotic stress tolerance,

Abstract Current definitions of essential or beneficial

elements for plant growth rely on narrowly

defined criteria that do not fully represent a new

vision for plant nutrition and compromise fertilizer

regulation and practice. A new definition of what is

a plant nutrient that is founded in science and relevant

in practice has the potential to revitalize innovation

and discovery. A proposed new definition might

read: A mineral plant nutrient is an element which is

needed for plant growth and development or for the

quality attributes of the harvested product, of a given

plant species, grown in its natural or cultivated environment.

It includes elements currently identified as

essential, elements for which a clear plant metabolic

function has been identified, as well as elements that

have demonstrated clear benefits to plant productivity,

crop quality, resource use efficiency, stress

Responsible Editor: M. Iqbal R. Khan.

P. H. Brown

Department of Plant Science, University of California

Davis, One Shields Ave, 95616 Davis, CA, USA

F.-J. Zhao

College of Resources and Environmental Sciences,

Nanjing Agricultural University, 210095,China Nanjing,

China

A. Dobermann (*)

International Fertilizer Association (IFA), 49 avenue

d’Iena, 75116 Paris, France

e-mail: adobermann@fertilizer.org

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Plant Soil

1 3

or improve the quality or nutritional value of the harvested

product.

In the science, regulation, commercialization and

use of fertilizers and other sources of plant nutrients

the definition of an ‘essential element’ has considerable

importance. Although no universally accepted

body exists for regularly reviewing and updating

the ‘established list’, for practical purposes 17 elements

are commonly classified as ‘essential’ for plant

growth, namely carbon (C), hydrogen (H), oxygen

(O), nitrogen (N), phosphorus (P), potassium (K), sulfur

(S), calcium (Ca), magnesium (Mg), chlorine (Cl),

boron (B), zinc (Zn), manganese (Mn), iron (Fe), copper

(Cu), molybdenum (Mo), and nickel (Ni). Others,

such as sodium (Na), silicon (Si), selenium (Se),

aluminum (Al), cobalt (Co) or iodine (I), are known

to also beneficially impact plant growth, but they are

relegated to a legal and practical ‘no man’s land’.

In most countries they cannot be legally referred to,

marketed or sold as plant nutrients. Historically that

has not always been the case. In the 19th century, pioneers

of the mineral nutrition of higher plants (e.g. de

Saussure, Boussingault, Sprengel, Liebig, Lawes and

Gilbert) were primarily interested in improving agricultural

growth through mitigating nutrient deficiency

(Nortcliff and Gregory 2013). Some elements deemed

quite essential by them (e.g. Si, Na) are nowadays

mostly in the no-man’s land area because definitions

and methodologies changed over time. In contrast,

research on essentiality proceeded much faster in

animal nutrition. By 1981, 22 mineral elements were

classified as essential for animal life, which also led

to significant improvements in animal diets and supplements

(Suttle 2010).

Science and practice of plant nutrition must refocus

on optimizing the full scope of food, socioeconomic,

environmental and health objectives necessary

to sustain a healthy global population and environment

(Scientific Panel on Responsible Plant Nutrition

2020). Many in the global scientific community,

as well as agricultural producers, policy makers and

industry who are engaged in agriculture, nutrition and

environment, have embraced this new vision but may

find the science of plant nutrition and its practical

implementation constrained by a too narrow definition

of a ‘plant nutrient’.

This opinion article is a call for new thinking that

begins with updating our understanding of what is a

plant nutrient. We propose a new definition for plant

nutrients merely as a starting point for further discussion.

We focus on the known chemical elements of

the periodic table which can be provided to the benefit

of crops grown in an agricultural setting, but we

also elaborate on possible further expansions of such

a debate and definition. We hope that by rethinking

the definition of a plant nutrient in the context of the

holistic goals of plant nutrition we can encourage a

new generation of plant nutrition researchers, spur

innovation in public and private sector, and sustainably

improve food systems.

Plant nutrients: a historical perspective

The beneficial effect of adding ash or other forms of

minerals to soils to improve plant growth has been

known for more than 2000 years, but it was mainly

in the 19th century that a broader understanding of

the role of different elements arose (Kirkby 2012).

Nicolas Théodore de Saussure was perhaps the first to

show that developing plants require mineral nutrients,

often in very small amounts, insisting that some elements

absorbed by plants were indispensable, while

others might not be essential (Saussure 1804).

Carl Sprengel, in a series of papers published in

the 1820 and 1830s, listed 20 elements that he considered

to be plant nutrients (Van der Ploeg et al. 1999).

Building on Sprengel’s work, Justus von Liebig erroneously

believed that the elemental composition in

plants was constant and could thus serve as a measure

of nutrient need (Liebig 1840; Macy 1936). Lawes

and Gilbert, however, demonstrated that neither the

presence nor the concentration of an element in a

plant could serve as a reliable indicator for its nutrient

needs or as a guide for its fertilizer needs (Lawes and

Gilbert 1851; Macy 1936). Nevertheless, by the end

of the 19th century, the value of adding certain elements

to crop production had been demonstrated and

farmers, particularly in Europe, were applying new

types of ‘mineral’ fertilizers to their crops (Kirkby

2012). The new plant nutrition findings also spread

quickly beyond Europe. For example, from 1882 to

1910, superphosphate was also almost universally

adopted by wheat farmers in South Australia (Byerlee

2021).

It became clear that a more precise study of

the essentiality of specific elements required new

techniques. Nutrient solution culture, first tried by

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Plant Soil

1 3

Boussingault around 1840 and further improved

in the 1850 and 1860 s by Sachs and particularly

Knop (Knop 1860), allowed for a more precise control

of nutrients under experimental conditions, and

thus became the principle method of plant nutrition

research. Sachs, in his first major book, states that one

cannot call a substance a plant nutrient just because

it is present in the plant (Sachs 1865). On pages 114-

115 he goes on proposing and elaborating two criteria

for distinguishing essential (“unenthbehrlich”)

from non-essential (“enthbehrlich, unnöthig”) plant

nutrients:

(i) a structural criterion: the element is an integral

component of the chemical formula of plant

substances, without which a cell cannot exist

(e. g., C, O, H, N, S);

(ii) a physiological criterion: demonstration that

the plant under otherwise good growth conditions

cannot complete its vegetation cycle without

uptake of any form of the element in question.

He pointed out, however, that testing for the second

criterion is experimentally challenging because it

is difficult to completely exclude a nutrient from the

system (including the seed). Nevertheless, applying

the second criterion, he concluded that the elements

K, Ca, Mg, Fe and P were also essential, whereas Na

and Cl appear to be non-essential. That, we dare say,

probably marks the origin of the strict definition that

is still in use today.

For a long time, it seemed that the list of essential

elements would remain at the 10 already mentioned

by Sachs in 1865, but it grew quickly in the 1920

and 1930s, when Mn (1922), B (1923), Zn (1926),

Cu (1931) and Mo (1938) were added to it (Kirkby

2012; Hoagland and Arnon 1948). To a large extent

this expansion resulted from improvement of analytical

methods and refinement of culture techniques,

particularly purification of nutrient solutions, as well

as widening the research to different plant species

that had higher nutrient requirements than others

(Hoagland and Arnon 1948). Terms such as micronutrients

or trace elements were coined during that time

too, to depict nutrients that were required only in very

small amounts in the physiology of the plant. The

question arose, which of those were indispensable to

growth or not. Motivated by that purpose, Arnon and

Stout (1939) postulated that a plant nutrient can be

considered essential only if

(i) “a deficiency of it makes it impossible for the

plant to complete the vegetative or reproductive

stage of its life cycle;

(ii) such deficiency is specific to the element in

question, and can be prevented or corrected

only by supplying this element; and.

(iii) the element is directly involved in the nutrition

of the plant quite apart from its possible effects

in correcting some unfavorable microbiological

or chemical condition of the soil or other culture

medium.”

One practical implication of this is that, based on

these criteria, a favorable response from adding a

given element to the growth medium does not constitute

conclusive evidence of its indispensability in

plant nutrition (Arnon and Stout 1939). The authors

were also aware of some of the theoretical and experimental

limitations of their definition, which also led

them to state, that, in principle, every element in the

periodic table may at some point be shown as being

essential to plants (Arnon and Stout 1939). Arnon

was also quite aware that different crops, different

stages and climatic factors can have different requirement,

and that the ‘essentiality’ definition is one of

strict physiological function, i.e. it does not necessarily

equate with agricultural requirement (Arnon

1952).

In 1952, Arnon proposed that rather than measuring

the effect of removal of a nutrient from the

medium, an alternative approach to asserting essentiality

could be to identify an essential cellular constituent

or biochemical reaction in which the element

participates (Arnon 1952). A more integrated concept

of essentiality would rest on the combined contribution

of physiological studies of growth and biochemical

studies of functions. Hence, the last criterion was

later re-phrased as “….its function or at least its direct

effect on the metabolism of the plant must be identified”,

and on that basis it was concluded that Na

meets the essentiality criteria in the freshwater algae

Anabaena cylindrica (Allen and Arnon 1955).

Establishing a requirement for minor elements

in plant metabolism thus became a fashionable

approach. Influenced by this evolution, but also by

findings that the 2nd criterion of Arnon and Stout

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Plant Soil

1 3

(1939) may be too rigid, the term functional nutrient

(or metabolism nutrient) emerged in contrast to

essential nutrient, to include any mineral element that

functions in plants irrespective of whether its action is

specific or indispensable (Nicholas 1961; Bollard and

Butler 1966). Interestingly, Nicholas also described

five types of experiments needed to establish unequivocal

evidence for minor elements to be classed

as functional constituents of enzymes. He also predicted,

that the agronomic importance of trace metals

will increase as less developed areas of the world

are brought into crop cultivation. It had become evident

that, particularly in the tropics and subtropics,

“deficiencies of minor elements in certain areas may

account for the disappointing results given by fertilizers

and the defective functioning of legumes, thus

preventing the establishment of stable systems of

farming’ (Webb 1959). This is an important point to

keep in mind for the debate we are proposing.

Around the same time, Epstein went on to reduce

the essentiality criteria to just two: (i) failure to grow

normally and to complete the life cycle in a medium

purged of the element (as in Arnon and Stout 1939)

and (ii) the element is a constituent of a molecule

which is known to be an essential metabolite (Epstein

1965). The latter transfers the test of essentiality

from the element itself to the metabolite of which it

is a part, which of course also has its own difficulties

(Epstein 1965). Hence, he also pointed out that

any such criteria of essentiality are mental constructs,

which are not easy to apply unambiguously in all situations

that exist in nature.

Over time, following the ‘functional’ notion, many

others have regularly reviewed the evidence for those

elements which do not clearly fail or pass the Arnon

and Stout criteria of essentiality (Bollard and Butler

1966; Asher 1991; Pilon-Smits et al. 2009; Subbarao

et al. 2003). Yet, after Cl was admitted in 1954, only

one new element was added to the list of essential

elements, Ni in 1987 (Kirkby 2012).

More recently, perhaps around the early 1980 s, the

term beneficial elements became popular to include

elements that stimulate plant growth or health, but

have not been shown so far to meet the strict essentiality

criteria (Asher 1991; Marschner 1986). Compared

to ‘functional’, ‘beneficial’ is perhaps more

meaningful in that it implies usefulness or importance

of some kind, but not necessarily essentiality, whereas

all essential elements are of course also functional.

Arnon had already recognized the many instances

where addition of an element might improve agricultural

production but not prove essentiality (Arnon

1952).

The definition of ‘essential’ and ‘beneficial’ mineral

elements has hardly changed since then. The

most recent edition of a leading textbook on plant

nutrition, Marschner’s “Mineral nutrition of higher

plants”, specifies that, for an element to be considered

essential, three criteria must be met (Kirkby

2012):

1. A given plant must be unable to complete its lifecycle

in the absence of the element.

2. The function of the element must not be replaceable

by another element.

3. The element must be directly involved in plant

metabolism – for example, as a component of an

essential plant constituent such as an enzyme – or

it must be required for a distinct metabolic step

such as an enzyme reaction.

Only the third criterion differs somewhat from

Arnon and Stout (1939), i.e. it represents a necessary

evolution in terms of integrating the biochemical role

of an element, as discussed above. In contrast, beneficial

elements are defined as elements that stimulate

growth, but are not essential according to these three

criteria, or are essential only for certain plant species,

or under specific conditions (Broadley et al. 2012).

The latter point, essentiality only in certain species

or under certain conditions, leaves much room for

interpretation. It may simply not be known yet, and

perhaps also causes great confusion among scientists,

regulatory bodies, industry and other stakeholders.

The distinction between beneficial and essential is

especially difficult in the case of some trace elements

(Broadley et al. 2012).

The consequences of not being a recognized plant

nutrient

Our concern is that the current definition of a plant

nutrient constrains the study of plant nutrition as well

as the development of fertilization practices needed

to optimize the production of foods ideally suited

for animal and human diets. Optimization of plant

nutrition in the context of a new societal optimum

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Plant Soil

1 3

for nutrients (Scientific Panel on Responsible Plant

Nutrition 2020) involves much more than the mere

ability to complete a plant’s lifecycle.

An important negative consequence of the historically

narrow definition of a plant nutrient has been

its use as the founding principle underlying the legal

definition of fertilizers and plant nutrients, as applied

by many regulatory agencies worldwide. The classification

of a nutrient as essential, as opposed to beneficial

or non-nutrient, profoundly affects all manner of

labeling, registration and use guidelines of fertilizers

and other nutrient-containing products. Plant nutrients

that are agronomically and economically critical

for plant development and growth and the production

of quality harvested product, but that are not called

‘essential’, currently fall into a regulatory limbo that

constrains scientific inquiry, limits industrial and

technological innovations and ultimately reduces

plant productivity and quality.

Just to serve as an example, Table 1 illustrates

the confusing discrepancy between elements that

are termed essential or beneficial nutrients by plant

nutritionists (Marschner 2012) and their respective

treatment in the current EU fertilizer regulation (EU

2019). In this example, Cl is listed as ‘essential’ by

plant nutrition scientists, whereas it is not classified

as a plant nutrient by the EU. In contrast, Co and Na

are viewed as ‘beneficial’ elements in science textbooks,

but classified as nutrients by the EU (Table 1).

As another example, the ISO standard on the classification

of fertilizers, soil conditioners and beneficial

substances (revised version currently under

development) strictly refers to the established list of

essential elements by defining micronutrient fertilizers

as “Fertilizers, which contain one or more of

the elements, such as boron, manganese, iron, zinc,

nickel, copper, molybdenum, and/or chlorine, which

are essential, in relatively small quantities, for plant

growth” (ISO 2021a). Similarly, the new ISO standard

on vocabulary defines ‘fertilizer’ as a “Substance

containing one or more recognized plant nutrient(s),

which is used for the purpose of providing the plants

or mushrooms with nutrients and designed for use or

claimed to have value in promoting their growth”;

it defines ‘plant nutrient’ as a “Substance, which

is essential for plant growth” (ISO 2021b). While

the vocabulary standard includes a definition of

‘other nutrient elements’ as “Substances that are not

required by all plants but can promote plant development

and may be essential for particular taxa.” (ISO

2021b), they are not included in the classification

system for fertilizers, soil conditioners and beneficial

substances (ISO 2021a). The ISO standards leave one

big question wide open: who ‘recognizes’ plant nutrients

as essential for plant growth?

In the United States, state agencies – not the federal

government – determine what is classed as a

nutrient, relying on advice from the research community.

The Association of American Plant Food Control

Officials (AAPFCO) strives to gain at least some

uniformity and consensus amongst the various U.S.

and Canadian fertilizer regulatory programs. As of

today, AAPFCO still primarily adheres to the Arnon

and Stout definition for nutrient essentiality.

At times this has bizarre consequences. For example,

although numerous reviews and hundreds of scientific

articles have been published on silicon’s beneficial

effects on plant growth, development, abiotic

and biotic stress, it is still not recognized as being

necessary for plant development by any of these bodies,

and thus also not widely used by farmers (Zellener

et al. 2021). It appears everyone is waiting for

each other to determine what is a plant nutrient and

what is not. In contrast, in 2004, the Brazilian Ministry

of Agriculture, which regulates commercial

production of fertilizers, ruled that Si is an essential

micronutrient (Zellener et al. 2021).

More than half of the elements in the periodic table

are known to occur in plant tissues and it is likely

that with improved analytical techniques many of

the remaining ones may be found too (Asher 1991).

Who is or can become the trusted global scientific

voice that judges if an element is a plant nutrient or

not, based on an updated view of the original criteria

Table 1 Current definition of selected elements as plant nutrients

(Marschner 2012) and their respective classification in the

current EU Fertilising Products regulation 2019/1009

Elements Marschner (2012) EU (FPR 2019/1009)

Al Beneficial Not a nutrient

Cl Essential Not a nutrient

Co Beneficial Nutrient

Na Beneficial Nutrient

Ni Essential Contaminant

Se Beneficial Not a nutrient

Si Beneficial Not a nutrient

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Plant Soil

1 3

set by agricultural scientists many decades ago? By

what authority can the currently accepted criteria be

updated to achieve the optimization of the full scope

of food, socioeconomic, environmental and health

objectives of a growing global population (Scientific

Panel on Responsible Plant Nutrition 2020)?

This discussion matters because an outdated, too

strict interpretation of the definition of a plant nutrient

impacts the entire human society. At the time of

Arnon and Stout (1939), global human population

was 2.3 billion and agricultural land was abundantly

(made) available. The current world population is

7.9 billion and future food production must primarily

rely on sustainable intensification of the existing land

(Folberth et al. 2020). Global climatic changes are

likely to result in more stressful conditions for crop

production, and there are significant needs and opportunities

to produce more nutritious food. We believe

that a modern definition of what is a ‘plant nutrient’

– grounded in science and relevant in practice – is

the foundation for a holistic crop nutrition contribution

to food system transformation and sustainable

development.

Some specific inadequacies of the current

definition of a plant nutrient

Concerns over the interpretation and negative impacts

of the strict definition of essentiality were eloquently

summarized by Epstein (1999) and others. In his

review of silicon, Epstein found the near-universal

acceptance of this definition to be puzzling in view of

its flaws, suggesting that for criterion (i) many plants

may be quite severely deficient in a nutrient element

and yet complete their life cycle; (ii) is redundant,

and (iii) presumes that designation of an element as

essential has to entail knowledge of its direct involvement

in the nutrition of the plant (Epstein 1999). As

an example, he pointed out that at the time when the

essentiality of boron was established (Brenchley and

Warington 1927), nothing was known about its direct

involvement in plant nutrition. Indeed, it was not until

1996 that the first definitive role of B was defined in

plants (reviewed in Brown et al. 2002). Prior to this,

the unambiguous evidence of essentiality was simply

that the plants failed unless the element was supplied.

The first criterion in the strict definition of an

essential nutrient – ‘A given plant must be unable to

complete its lifecycle in the absence of the element’

– would suggest that the ability to remove a putative

plant nutrient from the experimental environment

to such an extent as to disrupt the plant life cycle,

is the pre-requisite for the establishment of biological

essentiality. It is also worthwhile to mention that

such a strict criterion was never applied to defining

essential nutrients for animals and humans. This first

criterion suggests that essentiality is a matter of technological

capabilities and not biological function.

By this standard, the most recently identified essential

elements (e.g. B, Mo, Cl, Ni), which had been

known to be biologically important to plants, were

classified as ‘non-essential’ prior to the development

of the techniques required to eliminate trace contaminants

of these elements from the growth environment.

For some elements, e.g. iodine, even air purification

would be required to exclude the possible presence

of volatile forms of the element, a technique that

has not been implemented yet in current plant nutrition

research. Both Arnon and Stout (1939) and the

authors of Marschner (2012) book recognized that

the list of essential elements and the definitions will

change over time. They emphasized that the original

list of the ‘plant nutrients’ would and should expand,

i.e. developments in analytical chemistry and in

methods to minimize contamination during growth

experiments may lead to a lengthening of the list of

essential micronutrient elements and a corresponding

shortening in the list of beneficial elements.

Nickel is the most recent example of such development,

i.e. an example of the reliance upon new

technologies for chemical purification and experimental

cleanliness for eliciting deficiency symptoms

and functions. Nickel is now considered an essential

micronutrient for higher plants although failure to

complete the life cycle in the absence of Ni has only

been demonstrated in a few plant species (Gerendás

et al. 1999). It was initially considered because of

its specific function in the enzyme urease, but was

added to the list of essential nutrients after report of

a reduced germination capacity of Ni-deficient seeds

harvested from the third generation of Ni-deprived

plants grown in an ultra-clean culture environment

with extensive purification of nutrient salts (Brown

et al. 1987). Though failure to complete the plant

life-cycle has not been demonstrated in the field, Ni

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Plant Soil

1 3

deficiency has been demonstrated to so severely limit

the productivity of tree species in several geographies

to become economically non-viable (Wood et al.

2004).

A second inadequacy of the strict Arnon and Stout

definition is that it ignores the realities of modern

agricultural and horticultural production. For some

uses, completion of the growth cycle may not be economically

meaningful at all (e.g., leafy vegetables,

ornamental plants, forest species, landscape plants

etc.). Instead, the speed of growth, developmental

progression, tolerance to stress conditions, ability

to grow under specific environmental conditions, or

the production of quality plant products are essential

for economic viability. To suggest a nutrient is not

a ‘plant nutrient’ from a regulatory and commercial

perspective unless the plant lifecycle is completed,

even in the presence of clear evidence of biological

function and economic importance, artificially constrains

productivity and innovation. We do note however,

that Arnon and Stout (1939) originally defined

their first criterion as “a deficiency of it makes it

impossible for the plant to complete the vegetative or

reproductive stage of its life cycle”, whereas later on

this was reduced to just ‘life cycle’ as a whole.

Silicon is a clear example of an element that is

essential for the economically viable production of

several plant species but that has not been shown to

meet criterion 1 of the classic essentiality criteria.

Silicon is present in plants in amounts equivalent

to those of many macronutrients and evidence suggests

that it should be included among the elements

having a major bearing on plant life (Epstein 1999).

Silicon plays an important role in enhancing plant’s

resistance to numerous biotic (e.g. microbial pathogens,

herbivores) and abiotic (e.g. salinity, drought,

heavy metals, nutrient deficiency, etc.) stresses (Ma

and Yamaji 2008; Coskun et al. 2019). The majority

of studies demonstrate significant effects of Si on

measures such as growth, photosynthesis, enzyme

activities, ion and water transport only under stress

conditions (Coskun et al. 2019; Zellener et al. 2021).

This is further supported by most transcriptomic studies

which show large effects of Si on gene expression

under stress conditions, but very few effects in

the absence of stress (Coskun et al. 2019). It can be

argued that non-stress conditions do not really exist

for field crops, which inevitably will experience

some sorts of stress during their life cycle. For Si

accumulator crops such as rice (Oryza sativa), yield

benefits from Si fertilizer applications have been well

documented (Epstein 1999; Ma and Yamaji 2008).

Silicon uptake mutants of rice grow poorly under

field conditions (Tamai and Ma 2008). In fact, depletion

of plant available Si in paddy soils due to continuous

removal of Si by rice crops has been suggested

as a cause for declining rice yields in certain situations

(Savant et al. 1997).

Based on the current definition, iodine is also not

considered an ‘essential element’, but, because of its

biological functions may now be considered a plant

nutrient too. It is required as an inorganic antioxidant

in some algae (Küpper et al. 2008) and at least

30 crops have been described to positively respond in

terms of an increase of plant biomass to the addition

of iodine at micronutrient levels in nutrient solution

(Medrano-Macías et al. 2016). Iodine has been shown

to influence N uptake and metabolism, photosynthesis

(chlorophyll production, efficiency and CO2-

fixation

as carbohydrates in the leaves and fruits) and anti-oxidant

production and oxidative stress-signaling pathways

(Kiferle et al. 2021; Gonzali et al. 2017). Phenotypic

studies showed the positive effect of iodine in

the nutrient solution at micronutrient levels on plant

biomass development, timely flowering and fruit formation,

and stress resilience, compared to a nutrient

solution with iodine concentration below detection

level (Kiferle et al. 2021).

Arnon and Stout (1939) also made no claim or

specification that an essential element must be essential

for all species under all conditions and yet the

term ‘essential plant nutrients’ has become accepted

as applying to all plant species. This assumption has

resulted in some unusual outcomes. For example,

while Si meets the Arnon and Stout requirement for

essentiality in rice, horsetail (Equisetum) and perhaps

cucurbits and other Si rich species, and has very clear

biological benefit to a broad array of species, it is not

included in the list of essential elements in most modern

textbooks. A wider point to make here is that different

evolutionary clades of plants can display quite

distinct mineral compositions (Neugebauer et al.

2018; Jansen et al. 2002). Composition does not, of

course, equate to essentiality, but there is surely still a

lot to be learned beyond the small number of species

that are typically studied.

The third criterion is also problematic as it fails

to recognize that the growing conditions for the

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Plant Soil

1 3

species in their native environment might impose

a unique constraint that is uniquely overcome by

the uptake of a particular nutrient. In the absence

of the constraints present in the natural environment,

that same element may show no benefit and

hence, by this definition, could not be considered

essential. The particular inadequacy of this has

recently been illustrated for tea (Camellia sinensis),

a species that is adapted to acid soils, and for

which Al3+

is essential for root growth and development

in all the tested varieties. In the absence of

Al3+,

tea plants failed to generate new roots which

is clearly a requirement for normal growth, development

and ultimately plant survival (Sun et al.

2020). To suggest that the essentiality of an element

can only be established in the artificial circumstance

of a highly purified culture media, but

not in the natural growing conditions is problematic

as it is well known that the prevalent growing

condition can dramatically affect the sensitivity of

a species to a nutrient deficiency. Thus, Co, Ni and

Mo are required in greater amounts in N fixing species;

Ni is required in greater amounts when urea

or ammonia are the dominant N source; Si is highly

beneficial when Mn is present at toxic levels, and

so on.

Epstein (1999) also argued that the three

requirements for essentiality were redundant and

not reflective of the biological importance of several

elements. Selenium, for example, fulfills criterion

3 as it is present at the catalytic center of

several antioxidant enzymes, such as glutathione

peroxidase (Martins Alves et al. 2020; Fajardo

et al. 2014) and may play a wide variety of other

biological roles, particularly in stress tolerance

(Fichman et al. 2018). Iodine also appears to satisfy

criterion 2 and 3. It was recently demonstrated

that I uniquely up- or down-regulated 579 genes

and that Arabidopsis (Arabidopsis thaliana) contains

82 iodinated proteins in root and shoot, many

of which are involved in several fundamental biochemical

processes, and that is not observed when

the closely related halogen bromine is included in

the nutrient solution (Kiferle et al. 2021). While Si

may not meet criterion 3 strictly, the deposition of

Si in the apoplast forming an obstruction barrier

for biotic and abiotic stressors underpins many of

the reported functions of Si in plants (Coskun et al.

2019), and this role is biologically important.

Expanding the scope

A question may be raised as to whether we should

think even more broadly beyond the direct beneficial

or essential roles of mineral elements in plants as discussed

above. This could include a consideration of

the role that nutrients in the environment can play in

enhancing plant productivity even when that element

is not-essential and has no specific role in a plant metabolic

process. The comments made below are meant

to be provocative, indicating potential additional considerations

for a new definition over the longer term.

The establishment of the current essential plant

nutrients has largely been achieved by growing plants

in highly refined culture media under controlled

experimental conditions. This approach is fundamentally

divorced from the reality of agricultural production

or natural environments in which environmental

stress, nutrient interactions and the microbiome all

affect plant performance. At the time of Arnon and

Stout, little was known about the fundamental role

that the plant microbiome plays in plant productivity

and adaptation to stress. We now know that plantassociated

microbiomes confer fitness advantages to

the plant host, including growth promotion, nutrient

uptake, stress tolerance and resistance to pathogens

(Trivedi et al. 2020). Given the critical role the plant

microbiome plays in all that, one might hypothesize

that a nutrient ‘essential for the microbiome’ would

in turn also be critical for optimal plant productivity,

particularly under stress. Nutrient elements that

are essential for microbiome function, for which the

role of Co for rhizobium is an example, may in turn

influence plant microbiome activity and hence crop

productivity (Okamoto and Eltis 2011). Such effects

would also not readily be observed in the artificial

culture conditions usually employed in studies of the

essential elements.

Elements of interest that are known to have biological

function in a range of organisms include:

Br, which naturally occurs in 3200+ organo halogens

(Gribble 1999) from a variety of species and

is known to be essential for tissue development and

membrane architecture in animals (McCall et al.

2014); Co which is known to have a broad array of

functions in microbial and animal systems (Kobayashi

and Shimizu 1999); Se which is essential for

bacteria, animals and at least in some plants is beneficial

for plant growth (Gupta and Gupta 2017); I

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Plant Soil

1 3

and Si as described above; V (vanadium) which has

function in several nitrogen fixing bacteria and peroxidases

from many taxonomic groups (Tanabe and

Nishibayashi 2019).

Another consideration in the discussion of what

is a plant nutrient could relate to the question of

whether we define a plant nutrient as solely an inorganic

element, or as a simple molecule? In animal

and human biology the definition of a ‘nutrient’ is

far more inclusive than it is in plant nutrition. The

Merriam Webster definition of a nutrient is “a substance

that is needed for healthy growth, development,

and functioning”. This definition uses the

terminology ‘substance’ since it includes organic

nutrient substances required by heterotrophic organisms

that the organism itself cannot synthesize (proteins,

amino acids, fats, vitamins, minerals, carbohydrates

etc.).

In classical plant nutrition the term ‘plant nutrients’

generally refers to the known essential mineral

elements, either in their elemental state or as the

molecular form as acquired by the plant (e.g. nitrate,

ammonium, phosphate, borate/boric acid, molybdate,

sulfate etc.). In common usage, though not legal

usage, the term ‘beneficial plant nutrient’ could also

be used to describe elements that have a positive

effect on the healthy growth, development, and functioning

of the plant (e.g. I, Si, Co, Na). Central to the

definition of what is a ‘plant’ nutrient is the specification

that an element be required for life cycle completion.

This differs fundamentally from the definition of

nutrient as used in animal or human nutrition, which

does not specify that the organism cannot survive in

the absence of the nutrient, only that it will not be

‘healthy’.

There is also no current consideration that organic

molecules synthesized outside the plant may function

as ‘plant nutrients’ in the fashion that vitamins and

other organic molecules are considered as nutrients to

heterotrophs. Evidence of the clear stimulatory effects

of plant growth promoting rhizobacteria and growing

evidence that some biostimulants can stimulate plant

growth by means other than their essential nutrient

content (Du Jardin 2015; Yakhin et al. 2017) may

suggest that molecules synthesized ex-planta might

also function as plant ‘nutrients’. The possibility that

discrete organic molecules, or complex inorganic

molecules may be critical for plant growth and development

has not been rigorously explored, but should

at least be considered in the future, in the broad redefining

of what is a plant nutrient.

Although these are all worthy topics for further

debate, we propose to first focus attention on elements

of the periodic table and their direct role as

plant nutrients. Future definitions could also consider

other (mineral or organic) substances that have clear

beneficial effects on plants and their uses, or microbial

functions affecting plants.

Moving forward

The purpose of the proposed debate is not to re-define

the term ‘essential element’ (or essential plant nutrient).

Instead, we propose, perhaps for the first time,

to properly define the term ‘plant nutrient’, through a

single definition that encapsulates both elements that

are essential and beneficial for plants, as well as those

that are important for other uses, such as animal and

human nutrition. A proposed new definition might

therefore read:

A mineral plant nutrient is an element which is

needed 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.

This definition should be viewed as a starting point

for further debate, but it has some interesting features.

It includes (i) elements currently identified as essential,

(ii) elements for which a clear plant metabolic function

has been identified (even if the first criteria of failure

to complete the lifecycle has not been demonstrated),

as well as (iii) elements that have demonstrated clear

benefits to plant productivity, crop quality, resource use

efficiency, or plant stress tolerance. Besides emphasis

on plant biomass (yield), it also covers benefits in

terms of plant health (e.g. tolerance to abiotic stresses

or resistance to pests and diseases) and the quality of

the harvested commercial products for their different

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Plant Soil

1 3

end uses. This also provides a much needed opportunity

to link plant nutrition more directly to animal and

human nutrition, a requirement that was stated a long

time ago (Hoagland and Arnon 1948).

Reframing the definition around the term ‘plant

nutrient’ and emphasizing that this explicitly includes

both the essential and the demonstrated beneficial

mineral elements provides greater clarity. It will

enable regulators to consider the beneficial elements

as legitimate fertilizer components, while encouraging

more scientific inquiry for optimizing yield and

quality oriented plant production strategies in different

species and environments. It would likely also

increase commercial activity. None of this would

diminish the Arnon and Stout principles, but rigor

must be applied to avoid a flurry of unproven claims,

or ‘snake oils’ being sold. Hence, it is important that

the beneficial nutrients would need to satisfy clear

criteria and demonstration (likely for a specific species,

environment or function).

The definition allows for future discoveries of elements

and it includes the possibility that a plant nutrient

may have environmental and/or plant specificity,

such as Al3+

for tea in acid soils, Co or V for associative

N fixation, or Si or Se under stress conditions.

We propose an open scientific debate on the refinement

and implementation of this updated definition of

plant nutrients. Another key outcome of this debate

could be a more precise definition of the modern experimental

evidence required to classify an element as a

plant nutrient. Particular emphasis must be placed on

the concrete tests to perform for beneficial elements, but

there is also need to refine those for essential elements.

It has long been considered, for example, that Na and

Si should also be classed as essential plant nutrients as

essentiality has already been established in some plant

species (Kirkby 2012; Bollard and Butler 1966; Epstein

1999; Subbarao et al. 2003).

While such tests should continue to place the

major emphasis on the functions of nutrients in the

plant, they must also recognize that we may not

know the precise functions yet, even if we observe

clear benefits to the plant. The scientific community

should draw up a robust protocol for the necessary

tests to perform in the laboratory, the field and

natural environments, based on the most advanced

scientific methodologies and techniques. The tests

could include – besides the phenotypical response of

the plant to the addition or removal of the candidate

nutrient from its environment – also regulation of

gene-expression and post-translational responses

in the proteome, or changes in enzyme activity to

explain the observed phenotypical response.

An independent global body of scientists

– for example through the International Plant Nutrition

Council – could be given the mandate to periodically

review such new evidence, update the list of essential

and beneficial plant nutrients, and thus also guide policy

makers and industry more directly in making the

right decisions for improving nutrition. As the leading

global association with more than 400 members

encompassing all actors in the fertilizer value chain,

the International Fertilizer Association (IFA) could act

as an important stakeholder and facilitator of a platform

to implement the outcomes of these discussions.

We believe that a rethinking of the definition

of plant nutrients would lead to several positive

outcomes:

• Scientists will be incentivized to further look for

new plant nutrients and study their functions and

interactions with plant productivity and efficiency.

• The fertilizer industry will have greater opportunities

for differentiation of products, collaborative

research and business innovation.

• Farmers will be freed to more fully explore the

holistic vision of ‘plant nutrition’ that includes

integrated roles of plant nutrients on stress tolerance,

efficiency of resource use, crop quality and

whole system sustainability.

• Consumers will benefit from enhanced productivity

and food that could be a lot more nutritious.

• Regulators and government agencies will achieve

a more nuanced, integrative, adaptable and modern

interpretation of what is a plant nutrient.

We wish to invite everyone to participate in an open

discussion and share their general views and specific

suggestions at https:// www. sprpn. org/ debate, through

e-mails to the corresponding author, or through commentaries

in the journal. A wonderful example for

such a debate can be found in recent issues of the New

Phytologist. Lewis argued that an alternative interpretation

of published evidence suggests that B – listed as

an essential plant nutrient for nearly 100 years –would

not be in compliance with one of the criteria for essentiality,

but should instead be viewed as potentially

toxic (Lewis 2020b). Spirited, thoughtful responses

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Plant Soil

1 3

(González-Fontes 2020; Wimmer et al. 2020; Lewis

2020a; McGrath 2020) made it clear that there is still a

lot to be learned about this particular nutrient. However,

despite the excellent scientific discourse, the discussion

on B did not resolve the fundamental definition problem

we are hoping to tackle here.

Dedication

This paper is dedicated to Professor Emanuel Epstein,

a close colleague and mentor to one of the authors

(PHB) and a leading light in plant nutrition for more

than 80 years. Emanuel Epstein commenced his study

of plant nutrition in the illustrious laboratory of Dennis

Hoagland at University of California, Berkeley

in 1942 under the direction of Perry Stout, who with

Daniel Arnon had developed the 1939 definition of

nutrient essentiality that is the focus of this paper.

Professor Epstein joined the Department of Soils and

Plant Nutrition at the University of California at Davis

in 1958 where he continues to be actively engaged,

including reviewing and commenting on this manuscript.

Professor Epstein is nearing his 105th birthday.

He has made many seminal contributions to plant

nutrition, e.g., being the first to demonstrate that nutrient

ions are absorbed by plant roots in a fashion akin

to enzymatic catalysis, thereby initiating the study of

ion transporters in plants. Prof. Epstein has also made

many seminal contributions in the field of salinity

and was a leading force in the recognition of the critical

role of silicon as a plant nutrient. The lead author

(PHB) has had the pleasure of many spirited discussions

with Emanuel on how an adherence to the Arnon

and Stout principle of essentiality constrains the field

of plant nutrition.

It is an honor to offer this opinion paper as a tribute

to Professors Epstein’s many contributions the

field of plant nutrition.

Open Access This article is licensed under a Creative Commons

Attribution 4.0 International License, which permits

use, sharing, adaptation, distribution and reproduction in any

medium or format, as long as you give appropriate credit to the

original author(s) and the source, provide a link to the Creative

Commons licence, and indicate if changes were made. The

images or other third party material in this article are included

in the article’s Creative Commons licence, unless indicated

otherwise in a credit line to the material. If material is not

included in the article’s Creative Commons licence and your

intended use is not permitted by statutory regulation or exceeds

the permitted use, you will need to obtain permission directly

from the copyright holder. To view a copy of this licence, visit

http:// creat iveco mmons. org/ licen ses/ by/4. 0/.

References

Allen MB, Arnon DI (1955) Studies on nitrogen-fixing bluegreen

algae. II. The sodium requirement of Anabaena

cylindrica. Physiol Plant 8:653–660. https:// doi. org/ 10.

1111/j. 1399- 3054. 1955. tb077 58.x

Arnon DI (1952) Growth and function as criteria in determining

the essential nature of inorganic nutrients. In: Truog E

(ed) Mineral nutrition of plants. University of Wisconsin

Press, Madison, pp 313–341

Arnon DI, Stout PR (1939) The essentiality of certain elements

in minute quantity for plants with special reference to copper.

Plant Physiol 14:371–375. https:// doi. org/ 10. 1104/ pp.

14.2. 371

Asher CJ (1991) Beneficial elements, functional nutrients, and

possible new essential elements, Micronutrients in agriculture.

Soil Science Society of America, Madison, pp

703–730

Bollard EG, Butler GW (1966) Mineral nutrition of plants.

Annu Rev Plant Physiol 17:77–112. https:// doi. org/ 10.

1146/ annur ev. pp. 17. 060166. 000453

Brenchley WE, Warington K (1927) The role of boron in the

growth of plants. Ann Bot 41:167–187

Broadley MR, Brown PH, Cakmak I, Ma JF, Rengel Z, Zhao

FJ (2012) Chapter 8 – Beneficial elements. In: Marschner

P (ed) Marschner’s mineral nutrition of higher plants, 3rd

edn. Academic, Amsterdam, pp 249–269

Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu

H, Pfeffer H, Dannel F, Römheld V (2002) Plant Biol

4(2):205–223

Brown PH, Welch RM, Cary EE (1987) Nickel: a micronutrient

essential for higher plants. Plant Physiol 85:801–803.

https:// doi. org/ 10. 1104/ pp. 85.3. 801

Byerlee D (2021) The super state: the political economy of

phosphate fertilizer use in South Australia, 1880–1940.

Jahrb Wirtsch / Economic History Yearbook 62:99–128.

https:// doi. org/ 10. 1515/ jbwg- 2021- 0005

Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds

O, Ma JF, Kronzucker HJ, Bélanger RR (2019) The

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Plant Soil

1 3

controversies of silicon’s role in plant biology. New Phytol

221:67–85. https:// doi. org/ 10. 1111/ nph. 15343

de Saussure T (1804) Recherches chimiques sur la végétation.

Nyon, Paris

Du Jardin P (2015) Plant biostimulants: definition, concept,

main categories and regulation. Sci Hortic 196:3–14.

https:// doi. org/ 10. 1016/j. scien ta. 2015. 09. 021

Epstein E (1965) Mineral metabolism. Plant Biochemistry.

Elsevier, Amsterdam, pp 438–466

Epstein E (1999) Annual review of plant physiology and plant

molecular biology. Silicon 50:641–664. https:// doi. org/ 10.

1146/ annur ev. arpla nt. 50.1. 641

EU (2019) Regulation (EU) 2019/1009 of the European Parliament

and of the Council of 5 June 2019 laying down

rules on the making available on the market of EU fertilising

products. https:// eur- lex. europa. eu/ legal- conte nt/ EN/

ALL/? uri= CELEX% 3A320 19R10 09. Accessed 14 Oct

2021

Fajardo D, Schlautman B, Steffan S, Polashock J, Vorsa N,

Zalapa J (2014) The American cranberry mitochondrial

genome reveals the presence of selenocysteine (tRNASec

and SECIS) insertion machinery in land plants. Gene

536:336–343. https:// doi. org/ 10. 1016/j. gene. 2013. 11. 104

Fichman Y, Koncz Z, Reznik N, Miller G, Szabados L, Kramer

K, Nakagami H, Fromm H, Koncz C, Zilberstein A (2018)

SELENOPROTEIN O is a chloroplast protein involved

in ROS scavenging and its absence increases dehydration

tolerance in Arabidopsis thaliana. Plant Sci 270:278–291.

https:// doi. org/ 10. 1016/j. plant sci. 2018. 02. 023

Folberth C, Khabarov N, Balkovič J, Skalský R, Visconti P,

Ciais P, Janssens IA, Peñuelas J, Obersteiner M (2020)

The global cropland-sparing potential of high-yield farming.

Nat Sustain 3:281–289. https:// doi. org/ 10. 1038/

s41893- 020- 0505-x

Gerendás J, Polacco JC, Freyermuth SK, Sattelmacher B

(1999) Significance of nickel for plant growth and metabolism.

J Plant Nutr Soil Sci 162:241–256. https:// doi. org/

10. 1002/ (SICI) 1522- 2624(199906) 162: 3< 241:: AIDJPLN2

41>3. 0. CO;2-Q

González-Fontes A (2020) Why boron is an essential element

for vascular plants: A comment on Lewis (2019) ‘Boron:

the essential element for vascular plants that never was’.

New Phytol 226:1228–1230. https:// doi. org/ 10. 1111/ nph.

16033

Gonzali S, Kiferle C, Perata P (2017) Iodine biofortification of

crops: agronomic biofortification, metabolic engineering

and iodine bioavailability. Curr Opin Biotechnol 44:16–

26. https:// doi. org/ 10. 1016/j. copbio. 2016. 10. 004

Gribble GW (1999) The diversity of naturally occurring

organobromine compounds. Chem Soc Rev 28:335–346.

https:// doi. org/ 10. 1039/ A9002 01D

Gupta M, Gupta S (2017) An overview of selenium uptake,

metabolism, and toxicity in plants. Front Plant Sci 7:2074.

https:// doi. org/ 10. 3389/ fpls. 2016. 02074

Hoagland DR, Arnon DI (1948) Some problems of plant nutrition.

Sci Monthly 67:201–209

ISO (2021a) International Standard ISO/DIS 7851 Fertilizers,

soil conditioners and beneficial substances —Classification.

ISO. https:// www. iso. org/ stand ard/ 77570.

html. Accessed 14 Oct 2021

ISO (2021b) International Standard ISO/DIS 8157 Fertilizers,

soil conditioners and beneficial substances – Vocabulary.

ISO. https:// www. iso. org/ stand ard/ 80949. html. Accessed

14 Oct 2021

Jansen S, Broadley MR, Robbrecht E, Smets E (2002) Aluminum

hyperaccumulation in angiosperms: a review

of its phylogenetic significance. Bot Rev 68:235–269.

https:// doi. org/ 10. 1663/ 0006- 8101(2002) 068[0235:

AHIAAR] 2.0. CO;2

Küpper FC, Carpenter LJ, McFiggans GB, Palmer CJ, Waite

TJ, Boneberg E-M, Woitsch S, Weiller M, Abela R,

Grolimund D, Potin P, Butler A, Luther GW, Kroneck

PMH, Meyer-Klaucke W, Feiters MC (2008) Iodide

accumulation provides kelp with an inorganic antioxidant

impacting atmospheric chemistry. Proc Natl Acad

Sci 105:6954–6958. https:// doi. org/ 10. 1073/ pnas. 07099

59105

Kiferle C, Martinelli M, Salzano AM, Gonzali S, Beltrami

S, Salvadori PA, Hora K, Holwerda HT, Scaloni A, Perata

P (2021) Evidences for a nutritional role of iodine

in plants. Front Plant Sci 12:616868. https:// doi. org/ 10.

3389/ fpls. 2021. 616868

Kirkby EA (2012) Chapter 1: Introduction, definition and

classification of nutrients. In: Marschner P (ed) Marschner’s

mineral nutrition of higher plants, 3rd edn. Academic,

Amsterdam, pp 3–5

Knop W (1860) Über die Ernährung der Pflanzen durch wässerige

Lösungen bei Ausschluss des Bodens. Landw

Versuchsst 2:65–99

Kobayashi M, Shimizu S (1999) Cobalt proteins. Eur J Biochem

261:1–9. https:// doi. org/ 10. 1046/j. 1432- 1327.

1999. 00186.x

Lawes JB, Gilbert JH (1851) On agricultural chemistry, especially

in relation to the mineral theory of Baron Liebig.

J R Agric Soc 12:1–40

Lewis DH (2020) The status of boron as an essential element

for vascular plants: I. A response to González-Fontes

(2020) ‘Why boron is an essential element for vascular

plants’. New Phytol 226:1231. https:// doi. org/ 10. 1111/

nph. 16030

Lewis DH (2020) The status of boron in relation to vascular

plants. New Phytol 226:1238–1239. https:// doi. org/ 10.

1111/ nph. 16128

Ma JF, Yamaji N (2008) Functions and transport of silicon in

plants. Cell Mol Life Sci 65:3049–3057. https:// doi. org/

10. 1007/ s00018- 008- 7580-x

Macy P (1936) The quantitative mineral nutrient requirements

of plants. Plant Physiol 11:749–764. https:// doi.

org/ 10. 1104/ pp. 11.4. 749

Marschner H (1986) Mineral nutrition of higher plants. Academic,

London

Marschner P (ed) (2012) Marschner’s mineral nutrition of

higher plants, 3rd edn. Academic, Amsterdam

Martins Alves AM, Pereira Menezes Reis S, Peres Gramacho

K, Micheli F (2020) The glutathione peroxidase family

of Theobroma cacao: Involvement in the oxidative

stress during witches’ broom disease. Int J Biol Macromol

164:3698–3708. https:// doi. org/ 10. 1016/j. ijbio mac.

2020. 08. 222

McCall AS, Cummings CF, Bhave G, Vanacore R, Page-

McCaw A, Hudson BG (2014) Bromine is an essential

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Plant Soil

1 3

trace element for assembly of collagen IV scaffolds in

tissue development and architecture. Cell 157:1380–

1392. https:// doi. org/ 10. 1016/j. cell. 2014. 05. 009

McGrath SP (2020) Arguments surrounding the essentiality

of boron to vascular plants. New Phytol 226:1225–1227.

https:// doi. org/ 10. 1111/ nph. 16575

Medrano-Macías J, Leija-Martínez P, González-Morales S,

Juárez-Maldonado A, Benavides-Mendoza A (2016) Use

of iodine to biofortify and promote growth and stress tolerance

in crops. Front Plant Sci 7:1146. https:// doi. org/ 10.

3389/ fpls. 2016. 01146

Neugebauer K, Broadley MR, El-Serehy HA, George TS,

McNicol JW, Moraes MF, White PJ (2018) Variation in

the angiosperm ionome. Physiol Plant 163:306–322.

https:// doi. org/ 10. 1111/ ppl. 12700

Nicholas DJD (1961) Minor mineral nutrients. Annu Rev Plant

Physiol 12:63–90. https:// doi. org/ 10. 1146/ annur ev. pp. 12.

060161. 000431

Nortcliff S, Gregory PJ (2013) The historical development of

studies on soil-plant interactions. In: Gregory PJ, Nortcliff

S (eds) Soil conditions and plant growth. Wiley-Blackwell,

Chicester, pp 1–21

Okamoto S, Eltis LD (2011) The biological occurrence and

trafficking of cobalt. Metallomics 3:963–970. https:// doi.

org/ 10. 1039/ c1mt0 0056j

Pilon-Smits EAH, Quinn CF, Tapken W, Malagoli M, Schiavon

M (2009) Physiological functions of beneficial elements.

Curr Opin Plant Biol 12:267–274. https:// doi. org/ 10.

1016/j. pbi. 2009. 04. 009

Sachs J (1865) Handbuch der Experimental-Physiologie der

Pflanzen: Untersuchungen über die allgemeinen Lebensbedingungen

der Pflanzen und die Functionen ihrer

Organe. W. Engelmann, Leipzig

Savant NK, Datnoff LE, Snyder GH (1997) Depletion of plantavailable

silicon in soils: a possible cause of declining

yields. Commun Soil Sci Plant Anal 28:1245–1252

Scientific Panel on Responsible Plant Nutrition (2020) A new

paradigm for plant nutrition. Issue Brief 01. https:// www.

sprpn. org/ issue- briefs. Accessed 14 Oct 2021

Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium—

a functional plant nutrient. Crit Rev Plant Sci 22:391–416.

https:// doi. org/ 10. 1080/ 07352 68039 02434 95

Sun L, Zhang M, Liu X, Mao Q, Shi C, Kochian LV, Liao H

(2020) Aluminium is essential for root growth and development

of tea plants (Camellia sinensis). J Integr Plant

Biol 62:984–997. https:// doi. org/ 10. 1111/ jipb. 12942

Suttle NF (2010) Mineral nutrition of livestock, 4th edn. CABI,

Wallingford

Tamai K, Ma JF (2008) Reexamination of silicon effects on

rice growth and production under field conditions using a

low silicon mutant. Plant Soil 307:21–27. https:// doi. org/

10. 1007/ s11104- 008- 9571-y

Tanabe Y, Nishibayashi Y (2019) Recent advances in nitrogen

fixation upon vanadium complexes. Coord Chem Rev

381:135–150. https:// doi. org/ 10. 1016/j. ccr. 2018. 11. 005

Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plantmicrobiome

interactions: from community assembly to

plant health. Nat Rev Microbiol 18:607–621. https:// doi.

org/ 10. 1038/ s41579- 020- 0412-1

Van der Ploeg RR, Böhm W, Kirkham MB (1999) On the origin

of the theory of mineral nutrition of plants and the law

of the minimum. Soil Sci Soc Am J 63:1055–1062

von Liebig J (1840) Die Chemie in ihrer Anwendung auf Agricultur

und Physiologie. Verlag Vieweg, Braunschweig

Webb RA (1959) Problems of fertilizer use in tropical agriculture.

Outlook Agric 2:103–113. https:// doi. org/ 10. 1177/

00307 27059 00200 302

Wimmer MA, Abreu I, Bell RW, Bienert MD, Brown PH, Dell

B, Fujiwara T, Goldbach HE, Lehto T, Mock H-P, von

Wirén N, Bassil E, Bienert GP (2020) Boron: an essential

element for vascular plants: A comment on Lewis (2019)

‘Boron: the essential element for vascular plants that

never was’. New Phytol 226:1232–1237. https:// doi. org/

10. 1111/ nph. 16127

Wood BW, Reilly CC, Nyczepir AP (2004) Mouse-ear of

pecan: a nickel deficiency. HortSci 39:1238–1242. https://

doi. org/ 10. 21273/ HORTS CI. 39.6. 1238

Yakhin OI, Lubyanov AA, Yakhin IA, Brown PH (2017)

Biostimulants in plant science: a global perspective. Front

Plant Sci 7:2049. https:// doi. org/ 10. 3389/ fpls. 2016. 02049

Zellener W, Tubana B, Rodrigues FA, Datnoff LE (2021) Silicon’s

role in plant stress reduction and why this element

is not used routinely for managing plant health. Plant Dis.

https:// doi. org/ 10. 1094/ PDIS- 08- 20- 1797- FE

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