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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Infectious Plant Diseases: Etiology, Current Status, Problems and Prospects in Plant Protection</title><author><name sortKey="Nazarov, P A" sort="Nazarov, P A" uniqKey="Nazarov P" first="P. A." last="Nazarov">P. A. Nazarov</name><affiliation><nlm:aff id="AF1">Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, 119991 Russia</nlm:aff></affiliation><affiliation><nlm:aff id="AF2">Moscow Institute of Physics and Technology, Dolgoprudny, Moscow region, 141701 Russia</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Federal Scientific Vegetable Center, VNIISSOK, Moscow region, 143080 Russia</nlm:aff></affiliation></author><author><name sortKey="Baleev, D N" sort="Baleev, D N" uniqKey="Baleev D" first="D. N." last="Baleev">D. N. Baleev</name><affiliation><nlm:aff id="AF4">All-Russian Scientific Research Institute of Medicinal and Aromatic Plants, Moscow, 117216 Russia</nlm:aff></affiliation></author><author><name sortKey="Ivanova, M I" sort="Ivanova, M I" uniqKey="Ivanova M" first="M. I." last="Ivanova">M. I. Ivanova</name><affiliation><nlm:aff id="AF5">All-Russian Scientific Research Institute of Vegetable Growing, Branch of the Federal Scientific Vegetable Center, Vereya, Moscow region, 140153 Russia</nlm:aff></affiliation></author><author><name sortKey="Sokolova, L M" sort="Sokolova, L M" uniqKey="Sokolova L" first="L. M." last="Sokolova">L. M. Sokolova</name><affiliation><nlm:aff id="AF5">All-Russian Scientific Research Institute of Vegetable Growing, Branch of the Federal Scientific Vegetable Center, Vereya, Moscow region, 140153 Russia</nlm:aff></affiliation></author><author><name sortKey="Karakozova, M V" sort="Karakozova, M V" uniqKey="Karakozova M" first="M. V." last="Karakozova">M. V. Karakozova</name><affiliation><nlm:aff id="AF6">Center of Life Sciences, Skolkovo Institute of Science and Technology, Moscow, 121205 Russia</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">33173596</idno><idno type="pmc">7604890</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7604890</idno><idno type="RBID">PMC:7604890</idno><idno type="doi">10.32607/actanaturae.11026</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000565</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000565</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Infectious Plant Diseases: Etiology, Current Status, Problems and Prospects in Plant Protection</title><author><name sortKey="Nazarov, P A" sort="Nazarov, P A" uniqKey="Nazarov P" first="P. A." last="Nazarov">P. A. Nazarov</name><affiliation><nlm:aff id="AF1">Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, 119991 Russia</nlm:aff></affiliation><affiliation><nlm:aff id="AF2">Moscow Institute of Physics and Technology, Dolgoprudny, Moscow region, 141701 Russia</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Federal Scientific Vegetable Center, VNIISSOK, Moscow region, 143080 Russia</nlm:aff></affiliation></author><author><name sortKey="Baleev, D N" sort="Baleev, D N" uniqKey="Baleev D" first="D. N." last="Baleev">D. N. Baleev</name><affiliation><nlm:aff id="AF4">All-Russian Scientific Research Institute of Medicinal and Aromatic Plants, Moscow, 117216 Russia</nlm:aff></affiliation></author><author><name sortKey="Ivanova, M I" sort="Ivanova, M I" uniqKey="Ivanova M" first="M. I." last="Ivanova">M. I. Ivanova</name><affiliation><nlm:aff id="AF5">All-Russian Scientific Research Institute of Vegetable Growing, Branch of the Federal Scientific Vegetable Center, Vereya, Moscow region, 140153 Russia</nlm:aff></affiliation></author><author><name sortKey="Sokolova, L M" sort="Sokolova, L M" uniqKey="Sokolova L" first="L. M." last="Sokolova">L. M. Sokolova</name><affiliation><nlm:aff id="AF5">All-Russian Scientific Research Institute of Vegetable Growing, Branch of the Federal Scientific Vegetable Center, Vereya, Moscow region, 140153 Russia</nlm:aff></affiliation></author><author><name sortKey="Karakozova, M V" sort="Karakozova, M V" uniqKey="Karakozova M" first="M. V." last="Karakozova">M. V. Karakozova</name><affiliation><nlm:aff id="AF6">Center of Life Sciences, Skolkovo Institute of Science and Technology, Moscow, 121205 Russia</nlm:aff></affiliation></author></analytic><series><title level="j">Acta Naturae</title><idno type="ISSN">2075-8251</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>In recent years, there has been an increase in the number of diseases caused by
bacterial, fungal, and viral infections. Infections affect plants at different
stages of agricultural production. Depending on weather conditions and the
phytosanitary condition of crops, the prevalence of diseases can reach
70–80% of the total plant population, and the yield can decrease in some
cases down to 80–98%. Plants have innate cellular immunity, but specific
phytopathogens have an ability to evade that immunity. This article examined
phytopathogens of viral, fungal, and bacterial nature and explored the concepts
of modern plant protection, methods of chemical, biological, and agrotechnical
control, as well as modern methods used for identifying phytopathogens.
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Acta Naturae</journal-id><journal-id journal-id-type="iso-abbrev">Acta Naturae</journal-id><journal-id journal-id-type="publisher-id">ActaNaturae</journal-id><journal-title-group><journal-title>Acta Naturae</journal-title></journal-title-group><issn pub-type="ppub">2075-8251</issn><publisher><publisher-name>A.I. Gordeyev</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">33173596</article-id><article-id pub-id-type="pmc">7604890</article-id><article-id pub-id-type="doi">10.32607/actanaturae.11026</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject><subj-group><subject>Molecular Biology</subject></subj-group></subj-group></article-categories><title-group><article-title>Infectious Plant Diseases: Etiology, Current Status, Problems and Prospects in Plant Protection</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Nazarov</surname><given-names>P. A.</given-names></name><xref ref-type="aff" rid="AF1"></xref><xref ref-type="aff" rid="AF2"></xref><xref ref-type="aff" rid="AF3"></xref><email>nazarovpa@gmail.com</email></contrib><contrib contrib-type="author"><name><surname>Baleev</surname><given-names>D. N.</given-names></name><xref ref-type="aff" rid="AF4"></xref></contrib><contrib contrib-type="author"><name><surname>Ivanova</surname><given-names>M. I.</given-names></name><xref ref-type="aff" rid="AF5"></xref></contrib><contrib contrib-type="author"><name><surname>Sokolova</surname><given-names>L. M.</given-names></name><xref ref-type="aff" rid="AF5"></xref></contrib><contrib contrib-type="author"><name><surname>Karakozova</surname><given-names>M. V.</given-names></name><xref ref-type="aff" rid="AF6"></xref></contrib></contrib-group><aff id="AF1">Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, 119991 Russia</aff><aff id="AF2">Moscow Institute of Physics and Technology, Dolgoprudny, Moscow region, 141701 Russia</aff><aff id="AF3">Federal Scientific Vegetable Center, VNIISSOK, Moscow region, 143080 Russia</aff><aff id="AF4">All-Russian Scientific Research Institute of Medicinal and Aromatic Plants, Moscow, 117216 Russia</aff><aff id="AF5">All-Russian Scientific Research Institute of Vegetable Growing, Branch of the Federal Scientific Vegetable Center, Vereya, Moscow region, 140153 Russia</aff><aff id="AF6">Center of Life Sciences, Skolkovo Institute of Science and Technology, Moscow, 121205 Russia</aff><pub-date pub-type="ppub"><season>Jul-Sep</season><year>2020</year></pub-date><volume>12</volume><issue>3</issue><fpage>46</fpage><lpage>59</lpage><history><date date-type="received"><day>25</day><month>5</month><year>2020</year></date><date date-type="accepted"><day>30</day><month>6</month><year>2020</year></date></history><permissions><copyright-statement>Copyright ® 2020 National Research University Higher School of Economics.</copyright-statement><copyright-year>2020</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/2.0/"><license-p>This is an open-access article distributed under the terms of the
Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is
properly cited.
</license-p></license></permissions><abstract><p>In recent years, there has been an increase in the number of diseases caused by
bacterial, fungal, and viral infections. Infections affect plants at different
stages of agricultural production. Depending on weather conditions and the
phytosanitary condition of crops, the prevalence of diseases can reach
70–80% of the total plant population, and the yield can decrease in some
cases down to 80–98%. Plants have innate cellular immunity, but specific
phytopathogens have an ability to evade that immunity. This article examined
phytopathogens of viral, fungal, and bacterial nature and explored the concepts
of modern plant protection, methods of chemical, biological, and agrotechnical
control, as well as modern methods used for identifying phytopathogens.
</p></abstract><kwd-group kwd-group-type="author"><kwd>bacteria</kwd><kwd>fungi</kwd><kwd>viruses</kwd><kwd>pesticides</kwd><kwd>phytopathogen</kwd><kwd>selection</kwd><kwd>disease resistance</kwd><kwd>integrated pest management</kwd><kwd>biological control</kwd><kwd>agrotechnical control</kwd><kwd>plant immunity</kwd></kwd-group></article-meta></front><body><sec><title>INTRODUCTION</title><p>A plant is considered to be susceptible to infection if environmental factors
alter its physiological processes thus resulting in a disrupted structure,
growth, functions, or other parameters. Plant diseases are classified as
infectious and non-infectious depending on the nature of a causative agent. The
symptoms of the disease may depend on its cause, nature, and the location of
the impact site. The factors causing plant diseases can be of biotic and
abiotic nature. Non-infectious diseases are caused by unfavorable growth
conditions; they are not transmitted from a diseased plant to a healthy one.
Infectious diseases, on the contrary, can spread from one susceptible host to
another, since the infectious agent can reproduce in the plant or on its
surface.
</p><p>The signs of plant diseases include wilting, spotting (necrosis), mold,
pustules, rot, hypertrophy and hyperplasia (overgrowth), deformation,
mummification, discoloration, and destruction of the affected tissue. Wilting
results from the loss of turgor pressure in the cells and tissues. It is caused
by both abiotic and biotic factors. Spotting is mostly associated with the
partial death of plant tissues due to biotic factors. Mold and pustules occur
as a result of fungal damage to a plant. Rot leads to both the death of
intracellular contents (bacterial wet or fungal dry rot) and destruction of the
intercellular substance and cell membrane (fungal dry rot). Hypertrophy and
hyperplasia represent an excessive growth and proliferation of the affected
tissue caused by pathogens. Deformations (leaf wrinkling, twisting, and
curling; threadlike leaves, fruit ugliness, and double-floweredness) can be
caused by various biotic and abiotic factors due to an outflow of the products
of photosynthesis, uneven intake of nutrients by the plant, or uneven growth of
various tissue elements. In mummification, plant organs are damaged by the
fungal mycelium, which leads to plant shrinkage, darkening, or compaction.
Color changes usually occur due to chloroplast dysfunction and low content of
chlorophyll in the leaves, which manifests itself in the light color of some
leaf areas (mosaic discoloration) or the entire leaf (chlorosis) [<xref rid="R1" ref-type="bibr">1</xref>, <xref rid="R2" ref-type="bibr">2</xref>].
</p><p>Infectious agents can spread through the air, with water, be transmitted by
animals, humans, and remain infectious for many months or years. The natural
reservoirs of infectious agents are soil, water, and animals: especially
insects.
</p><p>Infectious plant diseases are mainly caused by pathogenic organisms such as
fungi, bacteria, viruses, protozoa, as well as insects and parasitic plants
[<xref rid="R1" ref-type="bibr">1</xref>]. With the development of agriculture,
infectious plant diseases have become an increasingly significant factor
affecting crop yield and economic efficiency. In the field environment, each
plant cultivated as a monoculture has uniform conditions and requirements for
planting, care, and harvesting, which leads to higher yields and lower
production costs than in polyculture [<xref rid="R3" ref-type="bibr">3</xref>].
Over the past half century, the use of modern technologies, including
cultivation of monocultures, has allowed us to reduce the amount of additional
land needed for food production. However, growing the same crop in the same
location year after year depletes the soil and renders it unable to ensure
healthy plant growth. Another crucial issue is the susceptibility of
monocultures to infectious diseases. Losses can amount to up to 30% even at the
stage of storage, transportation, and distribution to the consumer
(<italic><xref ref-type="fig" rid="F1">Fig. 1</xref></italic>)
[<xref rid="R4" ref-type="bibr">4</xref>, <xref rid="R5" ref-type="bibr">5</xref>]. Therefore, it is necessary to arrest or
prevent the development of infectious diseases at all stages of crop
production: starting from seed handling technologies and ending with the
delivery and storage of the product on store shelves and in consumers’
homes. This review summarizes existing data on the causes and pathogenetic
mechanisms of infectious plant diseases caused by viruses, bacteria, and fungi
that affect major agricultural crops, including cereals, vegetables, and
industrial crops. The article considers the current status, as well as the
problems and prospects of plant protection.
</p><fig id="F1" orientation="portrait" position="float"><label>Fig. 1</label><caption><p><italic>A </italic>- crop losses in industrialized countries (medium and high
per capita income) at each stage of the production process, starting from
cultivation and ending with consumption by households. The results present data
for three regions: 1 – Europe (including Russia), 2 – North America
and Oceania (USA, Canada, Australia, and New Zealand) and 3 – Industrial
Asia (Japan, China, South Korea). Losses are calculated by weight as a
percentage of the total mass of the product at the production stage [<xref rid="R4" ref-type="bibr">4</xref>]. <italic>B </italic>- top 10 most grown
crops in the world (by import). <italic>C </italic>- the most grown plant crops
in Russia. <italic>D </italic>- the main exported plant products from Russia
[<xref rid="R5" ref-type="bibr">5</xref>]
</p></caption><graphic xlink:href="AN20758251-12-03-046-g001"></graphic></fig></sec><sec><title>PLANT IMMUNITY AND MECHANISMS FOR ITS EVASION</title><p>Plants typically are resistant to non-specific pathogens thanks to the presence
of a waxy cuticle covering the epidermal cell layer and the constant synthesis
of various antimicrobial compounds. Specific pathogens use a variety of
strategies to penetrate plants, which often render such protection ineffective.
Fungi can penetrate directly into epidermal cells or form hyphae over plant
cells and between them, which does not require special structures or
conditions. Meanwhile, bacterial and viral infections often require either
damaged tissues, specialized structures (e.g., stomata) for entering the cell,
or a specific carrier (vector). The latter is usually an insect, a fungus, or
protozoa. How does plant infection with phytopathogens occur? In order to
understand this, it is important to keep in mind that, unlike animals, plants
rely on the innate immunity of each cell and systemic signals emanating from
the sites of the infection and not on mobile defense cells and the somatic
adaptive immune system. Moreover, an infection by pathogenic microorganisms is
not always successful because of the structural changes in the cell wall or
programmed cell death.
</p><p>Plants have so-called trichomes: outgrowths of the epidermis that prevent
pathogen growth and penetration. Trichomes may contain antimicrobial compounds
or exert an inhibitory effect on the microbial hydrolytic enzymes involved in
cell wall damage. The role of the cell wall cannot be overestimated: it is the
first obstacle that pathogenic microorganisms must evade; successful protection
at this line of defense is most effective against non-specific pathogens. The
cell wall consists of cellulose microfibrils and hemicellulose; it is
reinforced with lignin and contains a significant amount of proteins that
perform structural and enzymatic functions [<xref rid="R6" ref-type="bibr">6</xref>]. The heterogeneity of the structure of the plant cell wall
forces pathogens to use various strategies to penetrate it.
</p><p>Antimicrobial plant compounds, which contain low-molecular-weight non-protein
substances, are divided into two groups: phytoanticipins and phytoalexins.
Phytoanticipins, such as saponins, phenylpropanoids, alkaloids, cyanogenic
glycosides, and glucosinolates, are antimicrobial compounds pre-synthesized by
plants. Phytoalexins are formed in response to a pathogenic attack and include
various phenylpropanoids, alkaloids, and terpenes. An overlap between these
groups of antimicrobial agents is explained by the fact that the phytoalexins
of some plants can act as phytoanticipins in others [<xref rid="R7" ref-type="bibr">7</xref>]. In addition, small RNAs regulate the expression of a wide
range of genes in plants and comprise natural immunity against viruses [<xref rid="R8" ref-type="bibr">8</xref>]. Plants can also absorb and process
exogenous hairpin double-stranded RNAs (dsRNAs) to suppress the genes
responsible for the life maintenance and virulence of viruses pathogenic to
plants, fungi, and insects [<xref rid="R9" ref-type="bibr">9</xref>].
Aspartate-specific apoptotic proteases (phytaspases), which induce apoptosis,
the process of programmed cell death, play an important role in plant defense
[<xref rid="R10" ref-type="bibr">10</xref>].
</p><p>Plants have two types of immune system. The first one uses transmembrane
pattern recognition receptors that respond to slowly evolving microbial or
pathogen-associated molecular patterns, while the second one acts mainly inside
the cell using the polymorphic protein products encoded by most disease
resistance (R) genes [<xref rid="R11" ref-type="bibr">11</xref>].
</p><p>Plant R genes interact with the <italic>avr </italic>(avirulence) gene products
of the corresponding pathogens. In the presence of the corresponding R gene
encoding a receptor that triggers the defense response cascade, the receptor
recognizes the <italic>avr </italic>gene product and the plant exhibits a
resistance phenotype. For protection against bacterial, viral, and fungal
infections, as well as against insects, plants encode only eight classes of the
R gene products [<xref rid="R12" ref-type="bibr">12</xref>] that trigger the
downstream reaction cascade, which indicates degeneracy of the plant immune
system. The number of R genes in the genome can amount to about 100, which is
clearly not enough to recognize all possible pathogens. Apparently, recognition
of pathogens by the plant immune system is also of a degenerative nature [<xref rid="R13" ref-type="bibr">13</xref>].
</p><p>The general mechanism of protection against pathogens is, apparently, as
follows: during the first phase of an infection, receptors recognize
pathogen-associated molecular structures (for instance, flagellin) and trigger
an immune response to prevent colonization, which leads to the elimination of a
non-specific infection. A specific pathogen produces effector molecules that
interfere with the molecules of the immune response, which triggers the
so-called effector-mediated susceptibility in susceptible plants. In resistant
plants, the R gene products recognize effectors, with further formation of
effector-mediated resistance, which can trigger a hypersensitivity (programmed
cell death) response in the pathogen-infected area [<xref rid="R13" ref-type="bibr">13</xref>]. During the course of evolution, pathogens have developed
several strategies to suppress plant defense responses, such as altering the
programmed cell death pathway, inhibiting protective compounds in the cell
wall, as well as changing the hormonal status of plants and the expression
pattern of defense genes [<xref rid="R14" ref-type="bibr">14</xref>]. However,
the products of R defense genes against a viral infection can trigger a series
of responses at once. For instance, the defense against potato virus X first
starts with the inhibition of viral replication in the absence of a
hypersensitivity reaction, while overexpression of the <italic>avr
</italic>gene induces a hypersensitivity reaction, which renders the plant
extremely resistant to this virus [<xref rid="R15" ref-type="bibr">15</xref>].
</p><p>Plants can develop the so-called acquired resistance if the infection that
causes resistance in one part of the plant spreads to other parts. This fact
indicates that the signaling molecules can move from the affected area to other
cells and enhance immunity to the previously encountered pathogen. It should be
noted that acquired resistance is not a <italic>de novo </italic>acquired
resistance but an activation of the existing resistance genes in response to a
pathogenic attack. The cells accumulate salicylic acid and the various proteins
associated with pathogenesis (e.g., chitinase). Such acquired resistance is of
a temporary nature and can be both systemic and local [<xref rid="R16" ref-type="bibr">16</xref>].
</p><p>Symbiotic bacteria colonizing the rhizosphere antagonize soil pathogens through
various mechanisms: siderophores suppress plant pathogens by competing for
iron; antibiotics suppress competing microorganisms, while chitinases and
glucanases lyse microbial cells. Moreover, as a result of symbiosis with
bacteria, plants can develop another, extremely peculiar type of resistance:
induced systemic resistance, which is also mediated by salicylic acid,
ethylene, jasmonic acid, and lipopolysaccharides. In contrast to acquired
systemic resistance, induced systemic resistance provides non-specific
protection, has no dose-dependent correlation with the effect, does not affect
the pathogen directly, and does not depend on the proteins associated with
pathogenesis [<xref rid="R16" ref-type="bibr">16</xref>]. Instead, it is
determined by the plant genotype and can cause changes in plant metabolism,
leading to a general increase in resistance [<xref rid="R16" ref-type="bibr">16</xref>].
</p><p>Thus, understanding the mechanisms of plant defense and the pathways utilized
by phytopathogens to overcome that defense allows one to devise a systematic
approach to plant protection.
</p></sec><sec><title>THE MOST SIGNIFICANT PHYTOPATHOGENS</title><p><bold>Viruses and viroids </bold></p><p>Viruses are non-cellular infectious agents that can only replicate in living
cells. Viruses infect all types of organisms, from plants and animals to
bacteria and archaea [<xref rid="R17" ref-type="bibr">17</xref>]. They can be
integrated into the host’s genome and remain there as an inactive
provirus or actively replicate and regulate the host’s biosynthesis
processes. The suppression of viral gene transcription can lead to a latent
infection [<xref rid="R18" ref-type="bibr">18</xref>]. Plant viruses mainly
come in the form of single-stranded (ss) and double-stranded (ds) RNA viruses,
as well as single-stranded and DNA-containing retroviruses [<xref rid="R17" ref-type="bibr">17</xref>]. Due to a wide diversity of their genetic
material, the reproductive cycle and life pattern often vary from virus to
virus (<italic><xref ref-type="fig" rid="F2">Fig. 2A</xref></italic>).
Viruses are composed of a nucleic acid
molecule and a protective protein coat (capsid). Capsid can sometimes contain a
combination of proteins and lipids, which form a lipoprotein membrane. The
typical size of a plant virus is 30 nm [<xref rid="R19" ref-type="bibr">19</xref>].
</p><fig id="F2" orientation="portrait" position="float"><label>Fig. 2</label><caption><p><italic>A </italic>– plant viruses (and viroids): replication and
translation strategies. Tr – transcription, R – replication, RCR
– rolling-circle replication, T – translation, RT – reverse
transcription, E – encapsulation, ds – double-stranded, ss –
single-stranded, “–”– minus-strand,
“+”– plus-strand. <italic>B </italic>- schematic
representation of infection of neighboring cells by a virus (viroid) via
plasmodesmata. <italic>C </italic>- symmetric and asymmetric mechanisms of
viroid replication
</p></caption><graphic xlink:href="AN20758251-12-03-046-g002"></graphic></fig><p>The virion enters the cytoplasm of the plant cell via passive transport through
wounds caused by mechanical damage to the cuticle and cell wall, since it is
unable to pass through these structures on its own. Upon entering the cell, the
virus uncoats. DNA-containing viruses also need to penetrate the nucleus in
order to start transcription and mRNA synthesis. All viruses encode at least
two types of proteins: replication proteins, which are required for the
synthesis of nucleic acid, and structural proteins, which form the capsid. In
some cases, there are also proteins that are responsible for virion motility;
they ensure transport of virus particles between the plant cells. Viral
replication proteins bind to cellular proteins to form a complex that produces
multiple copies of the viral genome which interact with structural proteins to
form new virions, which are then released from the cell. This is the standard
viral life cycle.
</p><p>Plant viruses can be transmitted vertically (from parents to offspring) and
horizontally (from diseased plants to healthy ones). Viruses utilize small
intercellular channels called plasmodesmata to penetrate neighboring cells
(<italic><xref ref-type="fig" rid="F2">Fig. 2B</xref></italic>).
Viruses often express the proteins that ensure
virion motility by modifying channels to facilitate the transmission of the
infection to a neighboring cell [<xref rid="R20" ref-type="bibr">20</xref>].
This is how a local infection of a plant takes place. In order to infect an
entire plant, a virus must enter its vascular system, where it then moves
passively through the sieve tubes of the phloem with the flow of substances:
this is how it can infect cells distant from the primary site of the infection
[<xref rid="R19" ref-type="bibr">19</xref>, <xref rid="R20" ref-type="bibr">20</xref>].
</p><p>Some viruses are very stable and resistant to heat, can remain viable for a
long time in plant cells and the products derived from them [<xref rid="R21" ref-type="bibr">21</xref>, <xref rid="R22" ref-type="bibr">22</xref>], and can spread through passive mechanical transport from
one plant to another [<xref rid="R23" ref-type="bibr">23</xref>]. However, most
plant viruses actively spread from infected plants to healthy ones using a
carrier organism (vector). Carriers are divided into a mechanical vector, in
which the agent does not propagate, and a biological one, in which part of the
viral life cycle takes place [<xref rid="R24" ref-type="bibr">24</xref>]. The
main vectors of plant viruses are arthropods, nematodes, and fungi that feed on
plants [<xref rid="R25" ref-type="bibr">25</xref>].
</p><p>Plant viruses pose a serious threat to a wide range of crops, while the
economic losses caused by viruses are second only to the losses caused by other
pathogens [<xref rid="R26" ref-type="bibr">26</xref>]. Moreover, some viruses
can infect more than 1,000 different plant species comprising more than 85
families [<xref rid="R27" ref-type="bibr">27</xref>]. In the majority of
subtropical and tropical regions, a viral infection can lead to a loss of up to
98% of the crop [<xref rid="R28" ref-type="bibr">28</xref>]. Viruses manifest
themselves in a different way depending on the stage of crop production: they
can inflict colossal damage at the stage of crop growth, while at the stage of
harvesting, storage, and transportation, the damage from a viral infection is
minimal. It should be also noted that, in some cases, plants are found infected
with viruses in the absence of any obvious symptoms [<xref rid="R29" ref-type="bibr">29</xref>].
</p><p>The symptoms of viral diseases can be divided into five main types: growth
suppression (reduced growth of the entire plant or its leading shoots);
discoloration (mosaic, chlorotic rings, leaf chlorosis, variegation);
deformations (leaf wrinkling, corrugation, threadlike leaves); necrosis; and
impaired reproduction (flower sterility, parthenocarpy, shedding of flowers and
ovaries) [<xref rid="R2" ref-type="bibr">2</xref>].
</p><p>There is another type of infectious agents: viroids, which are circular RNAs
that cause various diseases in plants and animals. Taxonomically, they belong
to viruses (families <italic>Pospiviroidae </italic>and
<italic>Avsunviroidae</italic>). In contrast to viruses, viroids lack a protein
envelope (capsid) and present covalently linked ssRNA molecules 200–500
nucleotides long, which is 50-80 times shorter than the viral genome. Viroids
do not encode proteins and cannot replicate autonomously. It is considered that
the viroid can employ the DNA-dependent RNA polymerase, endoribonuclease, and
DNA ligase 1 (which is usually silent) of the host cell for its replication
[<xref rid="R30" ref-type="bibr">30</xref>]. Viroids replicate via a
rolling-circle mechanism, with members of the families <italic>Pospiviroidae
</italic>and <italic>Avsunviroidae </italic>replicating through an asymmetric
and symmetric pathway, respectively
(<italic><xref ref-type="fig" rid="F2">Fig. 2C</xref></italic>).
The molecular
mechanism of the pathogenic action of viroids is not fully understood. It is
believed that viroids can alter the phosphorylation state of gene products via
binding to cellular kinases [<xref rid="R31" ref-type="bibr">31</xref>], affect
the expression of the genes associated with growth, stress, development, and
protection [<xref rid="R32" ref-type="bibr">32</xref>], induce the proteins
associated with pathogenesis during an infection [<xref rid="R33" ref-type="bibr">33</xref>], cause post-transcriptional suppression of gene expression
by RNA interference, impair splicing [<xref rid="R34" ref-type="bibr">34</xref>], and induce demethylation of rRNA genes. It is surprising
that the substitution of one nucleotide at a certain position alters the
pathogenicity of the viroid significantly [<xref rid="R35" ref-type="bibr">35</xref>]. The RNA molecule of <italic>Pospiviroidae </italic>family
members has five domains: a central domain (C) containing the central,
conserved region, which plays an important role in viroid replication; a
pathogenicity domain (P) implicated in the manifestation of disease symptoms; a
variable domain (V), which is, apparently, responsible for viroid adaptation;
and the transport domains T1 and T2 (in cases of co-infection with two viroids,
they can exchange with these domains, which can contribute to their evolution).
Viroids of the family <italic>Avsunviroidae </italic>lack the central conserved
region but contain the sequences involved in the formation of the ribozyme
structures necessary for self-cleavage of RNA strands [<xref rid="R36" ref-type="bibr">36</xref>].
</p><p>The main symptoms of viroid diseases are reduced growth of the entire plant or
its parts, discoloration (chlorosis, anthocyanosis), and deformation of various
organs [<xref rid="R2" ref-type="bibr">2</xref>].
</p><p>Thus, viruses and viroids represent a rather large group of pathogens that
cause plant diseases and can result in serious damage to crops in the absence
of management and preventive measures, especially when infected at early stages
of plant growth.
</p><p><bold>Bacteria and phytoplasmas </bold></p><p>Bacteria are found almost everywhere and can be pathogenic to animals, plants,
and fungi [<xref rid="R37" ref-type="bibr">37</xref>]. Bacterial genetic
information is encoded in the DNA in the form of a chromosome; more than one
chromosome can be found in a cell. A bacterial cell can contain
extrachromosomal mobile genetic elements: plasmids that can carry important
virulence factors or, on the contrary, biological control factors. Bacteria can
also contain a prophage, which represents bacteriophage DNA integrated into the
genome. Most bacteria divide by binary fission, usually with simultaneous
duplication of both chromosomal DNA and extrachromosomal elements. Division of
a bacterial cell requires the presence of the membrane potential [<xref rid="R38" ref-type="bibr">38</xref>]. Bacteria can contain more than one
plasmid, since some of them can be lost during division. For instance,
<italic>Pantoea stewartii </italic>can harbor up to 13 different plasmids
[<xref rid="R39" ref-type="bibr">39</xref>]. Although bacteria usually transfer
plasmids within their population [<xref rid="R40" ref-type="bibr">40</xref>],
horizontal transfer of genetic information remains quite common in the
prokaryotic world.
</p><p>Bacteria have a cell membrane which separates the cytoplasm from the external
environment. Bacteria are divided into Gram-positive and Gram-negative
organisms depending on the cell wall structure [<xref rid="R41" ref-type="bibr">41</xref>]. The cell wall of Gram-positive bacteria consists of a
membrane and a thick peptidoglycan layer. The main component of the latter is
multilayered murein. Peptidoglycan also contains proteins, lipids, and teichoic
and teichuronic acids. The cell wall of Gram-negative bacteria has two
membranes with a peptidoglycan layer between them. The outer membrane contains
lipopolysaccharides and porins but lacks teichoic and lipoteichoic acids.
</p><p>Due to the presence of a cell wall, bacteria need secretion systems to pump out
xenobiotics, as well as release various proteins and virulence factors
(<italic><xref ref-type="fig" rid="F3">Fig. 3A</xref></italic>).
The secretion systems are divided into several
groups based on their structure. There are at least six different types of
secretion systems typical of Gram-negative bacteria, four types found in
Gram-positive bacteria, and two types present in both groups [<xref rid="R42" ref-type="bibr">42</xref>]. The secretion systems also play a key
role in the virulence of phytopathogenic bacteria. It should be noted that,
during the division of a bacterial cell, an asymmetry between mother and
daughter cells can be observed, where the mother cell retains most of the
secretion system transporters, while the daughter cell receives a smaller part
of transporters and is forced to synthesize them <italic>de novo
</italic>[<xref rid="R43" ref-type="bibr">43</xref>].
</p><p>As a rule, phytopathogenic bacteria grow more slowly than non-pathogenic ones
isolated from plants and have a temperature optimum of 20–30°C.
</p><p>Bacterial pathogens contain several types of genes: virulence genes, which play
a major role in infection and contribution to virulence, and disease-specific
genes, which are important for disease manifestation
(<italic><xref ref-type="fig" rid="F3">Fig. 3B</xref></italic>).
There are a series of genes that are required for host
recognition, pathogen attachment to the plant surface, formation of infectious
structures, as well as penetration and colonization of the host tissue.
Pathogenic factors may either remain attached to the bacterial surface or can
be released to the external environment. Pathogenic bacteria cause many serious
plant diseases around the world, although not as many as fungi or viruses;
however, the economic damage from bacterial diseases is relatively less severe
than that from fungi and viruses [<xref rid="R44" ref-type="bibr">44</xref>].
Bacteria wreak havoc at all stages of crop production. Furthermore, due to the
increase in the average annual temperature, there is reason to believe that the
damage from bacterial spot and economic loses will only continue to grow in the
coming years [<xref rid="R45" ref-type="bibr">45</xref>]. With an annual
increase in the average daily temperature in summer of 3–4°C, the
prevalence of bacterial diseases increases twofold, while the prevalence of
plant infection grows by 30–50% [<xref rid="R45" ref-type="bibr">45</xref>].
</p><fig id="F3" orientation="portrait" position="float"><label>Fig. 3</label><caption><p><italic>A </italic>– bacterial secretory systems that are used to infect
plant cells and tissues. <italic>B </italic>- development of bacterial
infection: 1 – penetration through the stomata due to phytotoxins, 2
– secretion of phytotoxins to modify the physiology, immune system, and
metabolism of plants, 3 – secretion of phytotoxins for degradation of the
cell wall and cytotoxic effect on plant cells, 4 – surface colonization
and formation of biofilms, 5 – damage to plant cells due to ice
nucleation and formation of crystals. <italic>C </italic>- development of
fungal infection: 1 – penetration into an intact cell at the site of
appressorium attachment through the combined effect of mechanical force and
enzymes that destroy the plant cell wall, 2 – penetration of the fungus
through stomata, 3 – secretion of phytotoxins to modify plant physiology,
immune system, and metabolism in biotrophic fungi 4 – penetration of the
fungus through the wound; 5 – secretion of phytotoxins for degradation of
the cell wall and cytotoxic effect on plant cells
</p></caption><graphic xlink:href="AN20758251-12-03-046-g003"></graphic></fig><p>There are two types of bacterial diseases: systemic bacterial blight
(penetration of the pathogen in the plant’s vascular system, its further
spread through the conductive bundles and adjacent tissues with disruption of
the normal process of water consumption) and local bacterial blight (damage to
the parenchymal tissues of individual plant organs). The main symptoms of
bacterial diseases are wilting, necrosis, chlorosis, rot, overgrowth (galls),
and scab.
</p><p>Phytoplasmas and spiroplasmas are two groups of very small (about 1 μm in
diameter) bacteria without a cell wall (they are separated from the external
environment by a cytoplasmic membrane). They cause phytoplasmosis and growth
retardation. Like mycoplasmas, a related genus of bacteria, phytoplasmas are
apparently one of the most primitive and autonomously reproducing living
organisms [<xref rid="R46" ref-type="bibr">46</xref>]. The genome of
phytoplasmas is 0.5–1.3 million bp [<xref rid="R47" ref-type="bibr">47</xref>], while the genome of <italic>Mycoplasma
genitalium</italic>, a model organism for studying the minimal genome,
comprises 0.58 million bp [<xref rid="R48" ref-type="bibr">48</xref>].
Phytoplasmas exhibit gliding motility [<xref rid="R49" ref-type="bibr">49</xref>], while representatives of the genus <italic>Spiroplasma
</italic>have a spiral shape and move in a twisting motion [<xref rid="R50" ref-type="bibr">50</xref>]. Cultivation of phytoplasmas in axenic
cultures is quite difficult, which indicates their greater dependence on the
host metabolism [<xref rid="R51" ref-type="bibr">51</xref>].
</p><p>Phytoplasmosis significantly decreases both crop yield and its quality. Crop
losses reach 40% for eggplants, 60% for tomatoes, 93% for pepper, 30–80%
for potatoes, and 100% for cucumbers [<xref rid="R52" ref-type="bibr">52</xref>]. Plants with phytoplasmosis are characterized by such
disorders of generative organs as virescence (greening of flowers and loss of
normal pigmentation), phyllodia (transformation of part of a flower into a
leaf-like formation), and proliferation (appearance of several
“pseudo” flowers instead of one). In addition, phytoplasmosis can
lead to the witches’ broom symptom (increased bushiness), dwarfism and
wilting of plants, as well as leaf deformations. There is only one known case
of positive phytoplasmosis, which leads to an economically useful effect: it is
phytoplasmosis of poinsettia, a popular seasonal ornamental plant.
</p><p><bold>Fungi </bold></p><p>Fungi are characteristic representatives of the domain Eukaryota. Unlike
bacteria, they have a complex cell structure with a distinct nucleus and
mitochondria. Fungal genome is much smaller than that of most eukaryotes but
much larger than prokaryotic. Fungi have a cell wall, which usually consists of
chitin, mannan, and chitosan, and also includes various proteins, lipids, and
polyphosphates. Fungi form a mycelium: a system of thin branching hyphae, which
sometimes lacks intercellular septa and forms a syncytium. Fungi are found in
all ecological niches and can cause significant harm. Fungi appear to be
evolutionarily much older than plants; the duration of their coexistence can be
compared to the evolutionary age of higher plants [<xref rid="R53" ref-type="bibr">53</xref>]. About 80% of the plants present on our planet to date are
symbiotic with fungi [<xref rid="R54" ref-type="bibr">54</xref>]. However,
fungi sometimes disrupt the delicate balance of the mutually beneficial
cooperation by turning into plant pathogens classified as biotrophs,
hemibiotrophs, and necrotrophs. As a rule, pathogenic fungi enter plants
through damaged leaves and stomata. However, in many cases, fungi secrete
specific infectious structures and enzymes that destroy a plant’s cell
wall (<italic><xref ref-type="fig" rid="F3">Fig. 3C</xref></italic>).
In the case of necrotrophs, which have a wide
range of hosts, the host cells die quickly from the combined action of enzymes
destroying the plant’s cell wall, reactive oxygen species, and/or toxins
[<xref rid="R55" ref-type="bibr">55</xref>, <xref rid="R56" ref-type="bibr">56</xref>]. Biotrophs, whose life cycle is associated with a living
host cell, secrete effector molecules that suppress the plant’s immune
system. These fungi exhibit specificity and interact with the host via special
biotrophic hyphae in the interphase region where biomolecules synthesized by
the plant are absorbed [<xref rid="R57" ref-type="bibr">57</xref>]. Fungi can
develop specific outgrowths of hyphae, so-called apressoria, which provide
attachment of the fungus to the substrate, thus allowing the pathogen to
penetrate the cell wall using a combination of mechanical force and enzymes
that degrade the plant’s cell wall. Haustoria move from the base of the
appressorium through the destroyed areas and penetrate the lumen. As a rule,
haustoria contain a large number of mitochondria and ribosomes with a
well-developed endoplasmic reticulum; haurtorium is usually separated from the
plant cell by invagination of the host plasmalemma [<xref rid="R58" ref-type="bibr">58</xref>]. At the same time, one can assume that an increased
pressure of plant defense can cause a transition from biotrophy to necrotrophy
[<xref rid="R53" ref-type="bibr">53</xref>].
</p><p>Phytopathogenic fungi are the most dangerous plant pathogens to cause harm at
all stages of crop production. The most common way to fight fungi is considered
to be treatment with fungicides. The use of fungicides is associated with
serious environmental and medical risks, namely the emergence of resistance and
horizontal transfer of resistance genes, with the occurrence of species with
multiple resistance [<xref rid="R59" ref-type="bibr">59</xref>]. At least 150
chemical compounds with different mechanisms of action are used as fungicides
in world agriculture; however, there have been cases of resistance among
various types of phytopathogens against almost all major classes of fungicides
recorded to date [<xref rid="R60" ref-type="bibr">60</xref>].
</p><p>The main symptoms of fungal diseases include wilting, spotting, mold (mycelium
and sporulation of the fungus on the surface of affected organs), pustules
(accumulation of fungal spores), overgrowth, deformations, mummification
(shrinkage, darkening, and compaction of the infected tissue), and rot [<xref rid="R2" ref-type="bibr">2</xref>].
</p><p>To date, more than 10,000 fungal species associated with plants have been
discovered, and it is not surprising that fungal infections cause more harm
than the diseases caused by other pathogenic microorganisms [<xref rid="R61" ref-type="bibr">61</xref>].
</p><p><bold>Complex diseases </bold></p><p>Although it is believed that a plant disease is caused by one pathogen species
or strain, microbes occur in nature mainly as part of complex multi-species
consortia/communities. Most laboratory studies focus on individual strains
grown in a pure culture. However, they cannot explain the complex course of
certain plant diseases. Therefore, the diseases where more than one pathogen is
involved are usually termed “complex” due to their complicated
diagnosis and subsequent control [<xref rid="R62" ref-type="bibr">62</xref>].
Synergistic interactions can occur between viruses, bacteria, fungi, and
different groups of pathogens. For instance, the synergism of virus–virus
type is observed when cowpea is co-infected with cowpea mosaic virus and
cucumber mosaic virus, with the severity of the disease and the degree of
growth retardation being greater than in the case of infection with individual
viruses [<xref rid="R63" ref-type="bibr">63</xref>]. Synergism of the type
bacterium–bacterium, which exacerbates the disease severity, can be
observed when tomato is co-infected with the bacteria <italic>Pseudomonas
corrugata </italic>and <italic>P. mediterranea</italic>, which cause tomato
pith necrosis [<xref rid="R64" ref-type="bibr">64</xref>]. Synergism of the
type fungus–fungus occurs quite often; it causes complex diseases such as
ascochyta blight complex of pea [<xref rid="R65" ref-type="bibr">65</xref>],
mango malformation disease [<xref rid="R66" ref-type="bibr">66</xref>], etc.
Brown apical necrosis of walnut resulting from the interaction of numerous
pathogenic fungi and bacterium <italic>Xanthomonas arboricola
</italic>represents an example of a synergistic interaction between different
groups of pathogens [<xref rid="R67" ref-type="bibr">67</xref>]. Synergism
between different pathogens resulting in more severe disease symptoms is more
common than expected and may be crucial in understanding microbial pathogenesis
and evolution, as well as further developing effective strategies of disease
management [<xref rid="R62" ref-type="bibr">62</xref>].
</p><p>Thus, phytopathogens are ubiquitous and cause various plant diseases
(<italic><xref ref-type="fig" rid="F4">Fig. 4</xref></italic>).
</p><fig id="F4" orientation="portrait" position="float"><label>Fig. 4</label><caption><p>Infectious plant diseases. From left to right, top row: tomato mosaic virus,
downy mildew of lettuce, bacterial blight of cauliflower, rye ergot, middle
row: potato spindle tuber viroid (William M. Brown Jr, amended), lettuce
bacterial blight, mixed viral infection on the ramson (cucumber mosaic virus,
tobacco rattle virus, tobacco mosaic virus), Septoria blight of celery; bottom
row: Fusarium blight of dill, onion rust, black rot (alternariosis) of carrots,
and tomato leaf curl virus
</p></caption><graphic xlink:href="AN20758251-12-03-046-g004"></graphic></fig><p><bold>Identification of phytopathogens </bold></p><p>Early diagnosis of plant diseases is a key factor that determines the timely
use of protective measures and, as a result, determines the yield and quality
of crop products. To date, in addition to conventional visual examination and
the method of indicator plants, serological methods and methods based on DNA
and RNA technologies are required in order to accurately identify plant
diseases. The most common methods of serological diagnosis include enzyme
immunoassay, immunoblotting, dot-blot hybridization, immunochromatography
[<xref rid="R68" ref-type="bibr">68</xref>], and serologically specific
electron microscopy [<xref rid="R69" ref-type="bibr">69</xref>]. Methods based
on DNA detection include fluorescence <italic>in situ </italic>hybridization
[<xref rid="R70" ref-type="bibr">70</xref>], various polymerase chain reaction
(PCR) techniques, including nested PCR, cooperative PCR, multiplex PCR,
real-time PCR, and DNA fingerprinting. There are also RNA-based approaches:
isothermal amplification of nucleic acids [<xref rid="R71" ref-type="bibr">71</xref>], the AmpliDet RNA real-time diagnostic system [<xref rid="R72" ref-type="bibr">72</xref>], and reverse-transcription PCR. These
methods allow for quick and accurate detection of the pathogen and
identification of its taxonomic rank. Novel approaches for a more accurate and
sensitive detection are now being developed. These are the next-generation
sequencing and metagenomic analysis, two-hybrid analysis, phage display, as
well as biosensor technologies based on electrochemistry and biophotonics
[<xref rid="R73" ref-type="bibr">73</xref>]. Thus, modern methods allow for
accurate identification of a phytopathogen even in the absence of infection
symptoms.
</p><p><bold>Integrated pest management (IPM) </bold></p><p>The system of managing the phytosanitary state of ecosystems using integrated
methods of pest management to ensure the phytosanitary prosperity of the
territory is effectively used in many countries [<xref rid="R74" ref-type="bibr">74</xref>].
</p><p>IPM is based on the assessment of an acceptable level of pests for determining
the pest threshold. A prerequisite for this is the constant monitoring of
pests, quarantine measures and seed purity, as well as the selection of
resistant varieties cultivated in the area. If the level of harmfulness is
reached, then methods of mechanical and biological control are mostly applied;
however, if necessary, chemical-control methods can be used in a responsible
and targeted manner.
</p><p>The costs of IPM and chemical management are practically comparable, while IPM
provides longer duration of the effect, increases yields by 10–30%,
improves product quality, reduces climate risks, and has a pronounced
environmental upside [<xref rid="R75" ref-type="bibr">75</xref>].
</p><p><bold>Seed reserves </bold></p><p>In the IPM paradigm, healthy planting material is a prerequisite for the
effective use of the system. Unfortunately, the seeds of most plants often
serve as reservoirs for various phytopathogens, and the infection can be
located both on the surface of the seed and inside of it. There are several
strategies for regulating the seed transmission of a pathogen existing to date:
the use of pathogen-free seeds and the search for methods of pre-sowing seed
treatment. The most effective way to combat fungi is considered to be treatment
of seeds with fungicides. Contact fungicides are used to destroy pathogens on
the seed surface, while translaminar fungicides can penetrate into the seed and
destroy the pathogen inside of it. These agents must act delicately to avoid
damaging the fetus [<xref rid="R76" ref-type="bibr">76</xref>]. In recent
years, there have been various strategies developed to control the pathogens on
seeds, including physical treatment (mechanical and thermal treatment,
ultrasonic and ultraviolet light exposure), treatment with natural compounds
and biological control agents, as well as substances inducing resistance [<xref rid="R77" ref-type="bibr">77</xref>].
</p><p>About 11 million tons of agricultural seeds are sown in Russia annually. The
volume rate of domestic seeds in the world’s cereal crops is 90%; it is
46% for corn, 43% for vegetables, 42% for soybeans, 32% for spring rape, and
26% for sunflower [<xref rid="R78" ref-type="bibr">78</xref>]. On the contrary,
the volume rate of foreign seeds used in Russia varies from 30 to 90% depending
on the culture, with the cost reaching 681,000 US dollars. The share of the
seed business in the total sales of large agrochemical companies such as
Syngenta, Bayer, DuPont, Dow, and Monsanto, is on the increase; they have
acquired seed companies and comprehensively expanded their research on crop
protection by developing and creating resistant varieties and hybrids using
modern high-end and high-performance technologies, including genome editing
[<xref rid="R79" ref-type="bibr">79</xref>].
</p><p><bold>Plant breeding and bioengineering </bold></p><p>Modern plant breeding for resistance to pathogens utilizes approaches and
methods of conventional and cell selection. The emergence of the complete
genomic sequences of some economically important crops now makes it possible to
effectively search for resistance genes, as well as the corresponding DNA
markers. Today, genetic markers based on DNA polymorphism (RFLP, RAPD, AFLP,
CAPS) and short tandem repeats (STRs, or SSRs), as well as DNA microarray
technology Diversity Arrays Technology (DArT) [<xref rid="R80" ref-type="bibr">80</xref>, <xref rid="R81" ref-type="bibr">81</xref>], are actively
used. A long-term increase in plant resistance can be achieved by using gene
pyramiding [<xref rid="R82" ref-type="bibr">82</xref>]; namely through the
development of genetically engineered varieties and distant hybridization
technology.
</p><p>Modern biotechnology approaches are becoming increasingly important for the
production of virus-resistant plant varieties and hybrids. Introduction of an
antisense gene in the plant for its modification allows one to disrupt viral
reproduction [<xref rid="R83" ref-type="bibr">83</xref>]. The gene encoding the
protein that has an affinity for viral RNA and inhibits its replication is also
inserted into the plant’s genome [<xref rid="R84" ref-type="bibr">84</xref>] to cause a delay in the expression of the transport
protein or a modification of plasmodesma [<xref rid="R85" ref-type="bibr">85</xref>]. Constant expression of chitinase or lysozyme of
bacteriophage T4 results in enhanced plant resistance to fungal and bacterial
infections [<xref rid="R86" ref-type="bibr">86</xref>, <xref rid="R87" ref-type="bibr">87</xref>]. Transgenic potato plants transcribing an RNA ribozyme
that cleaves the RNA minus-strand of the spindle tuber viroid have been
obtained [<xref rid="R88" ref-type="bibr">88</xref>].
</p><p>New breeding methods to select varieties resistant to plant pathogens include
powerful molecular tools for precise genetic modification, including the
CRISPR/ Cas9 system, which allows for more accurate genome editing than the use
of <italic>Agrobacterium</italic>-mediated transformation [<xref rid="R89" ref-type="bibr">89</xref>].
</p><p>Agrotechnical control is a mandatory component of the IPM system. Adequate
agricultural technology provides enhanced plant resistance to diseases and
prevents massive infection by creating optimal conditions for plant growth and
development. At the same time, crop rotation and selection of predecessors, the
system of soil cultivation, fertilizers, dates of sowing and harvesting, as
well as the destruction of weeds and post-harvest plant residues are of primary
importance [<xref rid="R90" ref-type="bibr">90</xref>]. Placement of
neighboring crops in the crop rotation and soil tillage are also essential
[<xref rid="R91" ref-type="bibr">91</xref>]. Destroying post-harvest residues
and weeds, which retain a large number of pathogens, while many weeds serve as
reservoirs for them, is also of prime importance.
</p><table-wrap id="T1" orientation="portrait" position="float"><label>Table</label><caption><p>The most significant phytopathogens
</p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="1" colspan="1">Viruses</th><th rowspan="1" colspan="1">Bacteria</th><th rowspan="1" colspan="1">Fungi</th></tr></thead><tbody><tr><td align="center" colspan="3" rowspan="1">The world’s most significant phytopathogens</td></tr><tr><td align="center" rowspan="1" colspan="1">Tobacco mosaic virus</td><td align="center" rowspan="1" colspan="1">Pseudomonas syringae</td><td align="center" rowspan="1" colspan="1">Magnaporthe oryzae</td></tr><tr><td align="center" rowspan="1" colspan="1">Tomato spotted wilt virus</td><td align="center" rowspan="1" colspan="1">Ralstonia solanacearum</td><td align="center" rowspan="1" colspan="1">Botrytis cinerea</td></tr><tr><td align="center" rowspan="1" colspan="1">Tomato yellow leaf curl virus</td><td align="center" rowspan="1" colspan="1">Agrobacterium tumefaciens</td><td align="center" rowspan="1" colspan="1">Puccinia spp.</td></tr><tr><td align="center" rowspan="1" colspan="1">Cucumber mosaic virus</td><td align="center" rowspan="1" colspan="1">Xanthomonas oryzae</td><td align="center" rowspan="1" colspan="1">Fusarium graminearum</td></tr><tr><td align="center" rowspan="1" colspan="1">Potato virus Y</td><td align="center" rowspan="1" colspan="1">Xanthomonas campestris</td><td align="center" rowspan="1" colspan="1">Fusarium oxysporum</td></tr><tr><td align="center" rowspan="1" colspan="1">Cauliflower mosaic virus</td><td align="center" rowspan="1" colspan="1">Xanthomonas axonopodis</td><td align="center" rowspan="1" colspan="1">Blumeria graminis</td></tr><tr><td align="center" rowspan="1" colspan="1">African cassava mosaic virus</td><td align="center" rowspan="1" colspan="1">Erwinia amylovora</td><td align="center" rowspan="1" colspan="1">Mycosphaerella graminicola</td></tr><tr><td align="center" rowspan="1" colspan="1">Plum pox virus</td><td align="center" rowspan="1" colspan="1">Xylella fastidiosa</td><td align="center" rowspan="1" colspan="1">Colletotrichum spp.</td></tr><tr><td align="center" rowspan="1" colspan="1">Brome mosaic virus</td><td align="center" rowspan="1" colspan="1">Dickeya dadantii</td><td align="center" rowspan="1" colspan="1">Ustilago maydis</td></tr><tr><td align="center" rowspan="1" colspan="1">Potato virus X</td><td align="center" rowspan="1" colspan="1">Dickeya solani</td><td align="center" rowspan="1" colspan="1">Melampsora lini</td></tr><tr><td align="center" rowspan="1" colspan="1">Citrus tristeza virus</td><td align="center" rowspan="1" colspan="1">Pectobacterium carotovorum</td><td align="center" rowspan="1" colspan="1">Phakopsora pachyrhizi</td></tr><tr><td align="center" rowspan="1" colspan="1">Barley yellow dwarf virus</td><td align="center" rowspan="1" colspan="1">Pectobacterium atrosepticum</td><td align="center" rowspan="1" colspan="1">Rhizoctonia solani</td></tr><tr><td align="center" rowspan="1" colspan="1">Potato leafroll virus</td><td align="center" rowspan="1" colspan="1">Clavibacter michiganensis</td><td align="center" rowspan="1" colspan="1"> </td></tr><tr><td align="center" rowspan="1" colspan="1">Tomato bushy stunt virus</td><td align="center" rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td></tr><tr><td align="center" colspan="3" rowspan="1">The most significant phytopathogens in Russia</td></tr><tr><td align="center" rowspan="1" colspan="1">Barley stripe mosaic virus</td><td align="center" rowspan="1" colspan="1">Candidatus Phytoplasma spp.</td><td align="center" rowspan="1" colspan="1">Alternaria solani</td></tr><tr><td align="center" rowspan="1" colspan="1">Wheat streak mosaic virus</td><td align="center" rowspan="1" colspan="1">Xanthomonas translucens</td><td align="center" rowspan="1" colspan="1">Fusarium avenaceum</td></tr><tr><td align="center" rowspan="1" colspan="1">Winter wheat Russian mosaic virus</td><td align="center" rowspan="1" colspan="1">Pseudomonas cichorii</td><td align="center" rowspan="1" colspan="1">Plasmopara halstedii</td></tr><tr><td align="center" rowspan="1" colspan="1">Oat Siberian mosaic virus</td><td align="center" rowspan="1" colspan="1">Rathayibacter tritici</td><td align="center" rowspan="1" colspan="1">Phytophthora infestans</td></tr><tr><td align="center" rowspan="1" colspan="1">Beet necrotic yellow vein virus</td><td align="center" rowspan="1" colspan="1">Pseudomonas fuscovaginae</td><td align="center" rowspan="1" colspan="1">Tilletia caries</td></tr><tr><td align="center" rowspan="1" colspan="1">Lettuce mosaic virus</td><td align="center" rowspan="1" colspan="1">Acidovorax citrulli</td><td align="center" rowspan="1" colspan="1"> </td></tr></tbody></table></table-wrap><p><bold>Chemical control </bold></p><p>Chemical control plays a crucial role in preventing losses associated with
plant diseases, especially with the advent of numerous fungicides with
selective toxicity, which expands possibilities for using them in targeted
fashion.
</p><p>The total cost of research, development, and registration of a new crop
protection product rose from USD 152 million in 1995 to USD 286 million in
2014. Worldwide sales have been increasing by about 6.5% annually since 1999
[<xref rid="R92" ref-type="bibr">92</xref>]. There are more than 600 different
chemical control agents on the market to date (fungicides, pesticides,
herbicides, nematicides, molluscicides, rodenticides, and antibiotics), and the
economic sector is now valued at more than USD 50 billion [<xref rid="R93" ref-type="bibr">93</xref>]. There are now strict regulations on the
use of chemical pesticides; and many products have been taken off the market,
banned or have failed to pass re-registration. For instance, six out of the ten
major chemical control products used in 1968 are currently banned as household
and agricultural pesticides in the United States.
</p><p><bold>Biological control and alternative to antibiotics </bold></p><p>Modern agriculture is becoming an increasingly high-end and multidisciplinary
industry with each passing year [<xref rid="R94" ref-type="bibr">94</xref>].
The uncontrolled use of herbicides leads to the appearance of populations of
weeds that are resistant to them [<xref rid="R95" ref-type="bibr">95</xref>].
Although success in disease management mainly depends on crop resistance and
the agricultural methods used, antibiotics such as gentamicin, oxolinic acid,
oxytetracycline, and streptomycin are widely used in crop production [<xref rid="R96" ref-type="bibr">96</xref>]. The use of antibiotics in crop production
is about 0.12%. However, in recent years, due to the widespread antibiotic
resistance, more emphasis has been placed on alternative forms of combating
phytopathogens. One such approach is the use of various methods of biological
control [<xref rid="R97" ref-type="bibr">97</xref>]. Examples of biological
control include the use of antagonist strains and antibiotic producers,
bacteriophages, insects for weed control, and parasitic insects for controlling
insect pests. For plant disease management, substances that are not themselves
representatives of the groups of antibiotics or antimycotics, such as
photosensitizers, bacteriophages, phagolysins, antimicrobial peptides, and
antibiofilm agents [<xref rid="R98" ref-type="bibr">98</xref>], are used. They
are especially useful if, in addition to antibacterial activity, they have
other properties, e.g., the ability to reduce the level of reactive oxygen
species or inhibit bacterial multidrug efflux pumps [<xref rid="R99" ref-type="bibr">99</xref>].
</p><p><bold>The most significant plant pathogens </bold></p><p>Several years ago, <italic>Molecular Plant Pathology </italic>conducted a
series of surveys among specialists in the field of molecular plant pathology,
which allowed the journal to select the ten most significant phytopathogenic
fungi [<xref rid="R100" ref-type="bibr">100</xref>],
viruses [<xref rid="R101" ref-type="bibr">101</xref>],
and bacteria [<xref rid="R102" ref-type="bibr">102</xref>]
(<italic><xref rid="T1" ref-type="table">Table</xref></italic>).
</p><p>One cannot but agree with such a choice. However, the structure of agricultural
products and crops grown in Russia differs from global ones and is
predominantly comprised of wheat, sugar beet, potatoes, barley, oats,
sunflower, and corn and, thus, requires adjustments to the list of pathogens
specific to these cultures [<xref rid="R2" ref-type="bibr">2</xref>, <xref rid="R65" ref-type="bibr">65</xref>, <xref rid="R79" ref-type="bibr">79</xref>,
<xref rid="R103" ref-type="bibr">103</xref>, <xref rid="R104" ref-type="bibr">104</xref>]<italic>. </italic></p></sec><sec><title>CONCLUSION</title><p>With the advent of modern diagnostic approaches, genome editing and sequencing
technologies, as well as microbiome and proteomic analysis methods, the study
of the mechanisms and effect of phytopathogens on plants has moved to a
multidisciplinary level. In this review, we have attempted to provide a
comprehensive picture of the current state of pest management. However, to our
deep regret, we could not consider many aspects of the interaction between
plants and phytopathogens, such as damage by ice nucleation proteins, which
cause the formation of ice crystals in plant cells [<xref rid="R105" ref-type="bibr">105</xref>] or the conserved nature of the sequences of effector
molecules in bacteria: pathogens of humans, animals, and plants [<xref rid="R106" ref-type="bibr">106</xref>].
</p></sec></body><back><ack><p>Acknowledgments: The reported study was funded by the Russian Foundation for
Basic Research (project number 19-116-50156).
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