in the interpretation
Linnaeus C. (1735,
1758): 2 evolutionary branches
nomenclature (genus, species)
- Owen R. (1858):
Haeckel E. (1866): 3 evolutionary
Pringsheim E. G. (1923): Bacteria
Copeland H.F. (1938): 4 evolutionary
Bacteria, Protista, Plantae, Animalia
Chatton E. (1938): 2 evolutionary
Phylogenomic - Molecular (RNAs, Proteins, Lipids) Comparative Approach
Zuckerkandl E. & Pauling L. (1965)
Stanier R. Y. (1971)
- Semantophoretic molecules
- (information carriers: genes,
- Episemantic molecules
(enzyme-catalyzed template-free syntheses)
- Asemantic molecules
Whittaker R.H. (1978): 5 kingdoms
Animalia, Plantae, Fungi,
- Divergence of Procaryotae at the
- of cellular evolution
Eubacteria + Archeobacteria
Woese C.R. et al. (1990): 3
E.G. & Hazen R.M. (2015)
Kang Liu et al. (2017)
- Geosphere and Microbiosphere in coevolution
Sourabh Jain et al. (2017)
- Plant Taxonomy based on comparative
analyses of primary and secondary metabolites
- New Order: Megavirales
- (genome size 100-2550 kB)
- acquisition and exchange of genes
in environmental interactions
E. & Pauling L. (1965): Molecules as Documents of Evolutionary
J. Theoret. Biol. 8: 357-366.
R.H. (1969): New Concepts of Kingdoms of Organisms
Science 163: 150-160.
C. R. Kandler O. & Wheelis M.L. (1990): Towards a natural system of
organisms: Proposal for the domains
Archaea, Bacteria, and
Proc. Natl. Acad. Sci. USA 87:
|Grosch E.G. & Hazen R.M.
(2015): Microbes, Mineral Evolution, and the Rise of
Microcontinents - Origin and Coevolution of Life with Early Earth
Astrobiology 15: 922-939.
|Cronin L. & Walker S.I.
(2016): Beyond prebiotic chemistry
Science 352: 1174-1175.
|Kang Liu et al. (2017): Novel Approach
to Classify Plants Based on Metabolite-Content Similarity
BioMed Research International
Volume 2017, Article ID 5296729
Jain et al. (2017): MimiLook: A Phylogenetic
Workflow for Detection of Gene Acquisition in Major Orthologous Groups
9(4): 72 doi:10.3390/v9040072
to Animal Kingdom, in Humans stress reactions leading to an adaptive new balance are subjective, cognitive processes
determined by the quality and duration of stress stimuli. Literature on phenotypic stress manifestations are huge encompassing stress responses characteristic of species (e.g. the human pattern of behaviour) or, of individuals belonging to it. Stress responses often end up in clinical manifestations and also, they have notable eco-evolutionary impact (traits influenced by polygenes
How is it with Plant Kingdom?
genes; the problem of genetic determination; mechanisms of cellular proteostasis and metabolic adaptation; intracellular redox systems).
Stress Adaptation in Plant Kingdom
Plant defensive and protective responses to simultaneous environmental stressors of biotic (pests, infective fungi, bacteria, viruses) and abiotic (climate extremes, soil physico-chemical changes, changes in air composition, geological events) origins may manifest either in tolerance, or resistance, or avoidance, or escape.
As for terrestrial plants fixed in the soil, escape responses deem to not applicable when coping with stress stimuli.
When it comes to defensive responses provoked by diverse stressors, single gene and polygene expressions influencing plant growth and physiological machinery are sharply modified leaving room for metabolic reactions required for self-sustaining in short term acclimatization or long term adaptive survival.
The evolutionary example of plant stress adaptation spanning multitude of generations is symbiosis
Elements in Plant Defense and Immunity
- structural elements (>>> indent
- recognition of the pathogenic elicitor molecular pattern
gene product R >< pathogen gene product avr)
- pathogenic transcriptional and
posttranscriptional gene silencing (RNA interference)
- stress-activated transcription factors
- polygenic resistance: some major genes (qualitative resistance) and series of minor genes
- postreceptor signalling in regulated cell death
- plant enzymes degrading pathogens
(chitinase, glucanase...), toxins, heat shock/stress proteins
- auxins, gibberellins, cytokinins interacting
with stress-activated plant hormones, peptides
- secondary metabolites → calcium,
oxygen intermediaries, abscisic acid,
salicylic acid, jasmonates, polyamines,
ethylene... in accumulation, interactions
- specific and nonspecific local prompt hypersensitive responses → secondary metabolites inducing acquired systemic resistance
As for Anton
de Bary (1879) the term symbiosis denotes cohabitation of living organisms from diverse species (2). Later on, studies modeling hosts and
symbionts in interactions and studies into game theories have led Maynard Smith and
(1990s years) extend the interpretation therefore, the term symbiosis covers the coexistence of all organic forms (living organisms, viruses, viroids,
capable to apply processes associated with the coexistence (2).
Important to note that in this extended
interpretation symbiosis and mutualism (+/+ reciprocity) have been
separated, further, besides
symbiotic interactions classified by benefits and
mutualism), the concept of "mere coexistence" with no classification has been introduced.
Taken together, it is questionned if symbiosis is a condition, a complex operating system, or both,
by interactions among the habitat, the environment, the symbiont
host genome either stress-compatible or stress-incompatible.
- coming up as result of stochastic interactions among the habitat, the environment, the symbiont host genome either stress-compatible or stress-incompatible.
in Plant Kingdom
For Search by Keywords:
(Journal of the American Society of Plant
As is known, it is about 400 million years ago, in the beginning of the Devon (Paleozoic) period that rudimentary signs of symbiosis (a kind of biotic stress) had been established
among parasitic fungi and host plants on their evolutionary way in landing. In result, terrestrial vascular plants (provided with xylem and phloem in the stem) widespread on Earth usually go into symbiosis (in plant root vertical articulation it is the absorptive hairy zone) with fungal hyphae in the soil. The symbiont association manifests in patterns of ectomycorrhiza (rich network of hyphae mantling host root surface and reaching out the neighbouring soil region), or endomycorrhiza (vesicular or arbuscular mycorrhiza; lattice of fungal hyphae penetrating cortical cells beneath host root epidermal cells), or ectendomycorrhiza (lattice of soil fungal hyphae penetrating intercellular spaces beneath host root epidermis). In fact, the evolution of plant-fungal symbiosis has picked up features of stress adaptation with bidirectional molecular communications between partners of former parasitic interactions, to yield in symbiotic common spaces handling common transport processes (transport of photosynthetic products to fungi,
transport of water and minerals to host plants) ensuring reciprocal survival (3,4,7,12,13).
As is known, it is about 100 million years ago, in the Cretaceous (Mesozoic)
period, that soil bacteria had adopted the purposeful molecular communications of symbiont fungi for developing symbiosis with Leguminosae (7,13,15).
Agrobotanical research of our days seeks for the molecular features, signalling pathways, phylogenetic
and phylogenomic correlations determining and influencing the development and process of symbiosis established by Leguminosae (Fabales) with soil bacteria (14-15,18-24). From point of agricultural application with emphasis on agro-regions suffering from intense agrochemical interventions
and from extreme climate circumstances, the transfer of symbiotic
processes into crops may open the way to soil bioregeneration and also, to safe cultivation of crops less dependent on soil nitrogen content (9,16,17,22-29).
|Ancient Rome had learnt cultivation techniques crop rotation
and green manuring from Egypt. Green manuring served for enriching soil with
nutrients (proteins, carbohydrates, lipids) of harvest recycled.
After a historic break in Europe, from the 19th century on, green
manuring joined again the collection of agrotechnical tools.
In human nutrition the primary food source are grains (grains/cereals, mainly Family Gramineae: wheat, barley, rice...); second to them are the nutritive Fabales (Families Fabaceae, Leguminosae: lupine, beetle, beans, peas..). Since macroelement nitrogen is essential for plant growth and crop formation, Gramineae vulnerable to soil nitrogen content mostly require the support of agrochemical fertilization. However, the last decades gave regrettable evidence on agrochemical fertilization quite detrimental to the ecosystem.
Unlike Gramineae, the role of Fabales in global (N2) traffic provided them with the eco-evolutionary advantage of living independently from soil nitrogen content. How could this happen and happened ever since?
For binding atmospheric nitrogen (N2-fixation) plant nodulation is necessary
but not sufficient as alone
(1,5,8-11,14-21,28,29) THE PHENOMENON (1,2,5,6,8)
Gram-negative Rhizobium soil bacteria (phylum Proteobacteria > polyphyletic classes Alphaproteobacteria,
Betaproteobacteria > polyphyletic ordos > polyphyletic families
> genera Allorhizobium,
Azorhizobium, Bradyrhizobium, Ensifer, Mesorhizobium, Rhizobium,
cluster on root zone (the hairy absorptive zone) of selected Leguminosae, then plant root hairs' ends curle up to become a bacterial trap. Thereafter plant root cortical cells divide
(polyploid cells), a new organ is formed (organogenesis) and evolves until environmental impulses keep on (> positive
feedback: low nitrogen and oxygen content, relatively high phosphorus content in the vicinity of the root -in the rhizosphere-...). High nitrogen and oxygen content, phosphorus deficiency (> negative feedback) in the rhizosphere lead to stop in development and also to controlled death of the newly formed organ.
Rhizobium bacteria clustered on selected plant root zone
penetrate the above mentioned cortical cells, they proliferate into so called
'infection tube' enveloped in cell wall for reaching more and more cell layers in the developing nodule
. Later on, membrane (plant cell membrane) enveloped bacteria exit the 'infection tube', enter nodule cell cytoplasm (endocytosis and symbiosome formation) and differentiate into endosymbiont bacteroids. If
differentiated, bacteroids lose the ability of division and
locomotion, they turn elongate and begin to bind atmospheric N2 (bacterial enzyme nitrogenase + atmospheric N2 ➨ ammonia synthesis ➨ permeation through peribacteroid membrane ➨ entry into host plant assimilation) and receive carbon skeleton (in compund) synthesized in dark phase of host plant photosynthesis.
The economic balance of the N2-binding legumerhizobium symbiosis: providing symbiont host plant with nitrogen (in compound), providing endosymbiont bacteroid with carbon skeleton (in compound). The energy cover of legumerhizobium development and operation within an adaptive and stress-free environment (nodule niche) is ensured by the host plant.
The development and operation of N2-binding
legumerhizobium symbiosis results from energy, time and
space-demanding molecular communications accompanied by reciprocal differentiation
of the interacting eukaryotic and bacterial partners. Decisive steps of molecular communication include:
Rhizobium soil bacteria (hereinafter referred to as rhizobium or bacteria) select adequate leguminous host plant, then in response leguminous host plant (hereinafter referred to as légume) selects adequate rhizobium soil bacteria.
The mechanism of mutual choice: chemotaxis
➥} interaction is
based on reciprocal and sequential gene induction, at the beginning of
which signaling substances in the selected légume rhizosphere (secondary metabolites: polyphenols ...) exert induction on rhizobium nod
In response: Rhizobium nod gene products' inductive effect on légume nodulin genes (nodulation).
Légume nodulin gene products
induce rhizobium nif genes:
➨ induction of metalloenzyme
nitrogenase (reductase component Fe-protein + catalytic
component Fe-Mo protein) ➨ diffusion of
and turn into ammonia ➨
bacteroid differentiation ➨ auxotrophism achieved by inhibiting bacterial ammonia-assimilation, hence, it is only the host plant NH3/NH4 assimilation in charge of providing N-compounds for partners in symbiosis.
microaerobic circumstances in the symbiotic nodules may promote
oxidation of iron-molybdenum cofactor in metalloenzyme nitrogenase, leading to enzyme inactivation. However, this kind of enzyme inactivation is prevented by fix operon cooperating with nif operon. Induction of fix genes provides the balanced operation of electron transport and redox systems (flavoprotein, ubiquinone oxidoreductase, ferredoxin homologues) affecting cellular respiration.
Example for the above process
Decisive steps in developing symbiosis of légume (
➾alfalfa Medicago sativa,
Medicago truncatula) with rhizobium (
- ➾Plant flavonoids discharged into légume rhizosphere.
- ➥ Flavonoid sensor receptors (NodD) on bacterial surface;
activation of postreceptor signaling pathways.
- ➥ Activation of bacterial nod (nodulation) genes.
- ➥ nod gene activation: synthesis of bacterial Nod
lipochito-oligosaccharide, wherein individual substituents on the
conserved chitin skeleton and, saturation and chain length
of fatty acid content determine the chemotactic decision, i.e.
host plant specificity).
- ➥ Achieving critical [picomolar-nanomolar] concentration of [Nod factor] in the rhizosphere.
- ➾ Critical [Nod factor] concentration perceived by symbiosis-specific receptor kinases on légume root hairs' cortical cell surface.
- ➾ Upon percieving critical [Nod factor] concentration, intracellular [Ca2+] oscillation and
Ca2+ influx into the cell are provoked by symbiosis-specific receptor kinases
of root hairs' cortical surface. In the following, Cl- and K+ efflux, transient depolarization of the plasma membrane, local rearrangement of the cytoskeleton take place, resulting in curling up of root hair tips for bacterial passage to go on, finally, for establishing bacterial trap (bacterial entry and proliferation in the cells = infection).
- ➾Légume early nodulin gene induction
(early nodulins = ENODs).
- ➾Inward growth of polarized "infection tube" in root hair tips, elongation of "infection tube" depending on the presence and concentration of Nod
factor and légume hormones, signalling molecules.
- ➥ Bacterial proliferation.
- ➾Plant hormones (auxin, cytokinins) induced cortical cell proliferation in légume root zone, nodulation-organogenesis (indeterminate or determined due to the presence or absence of meristemic cells, respectively).
- ➾Growing-lengthening of the "infection tube", ramification > elaboration of "infection tube" network accessing rudimentary nodules.
- ➥In support of bacterial and/or ➾légume enzymes degrading pectin and cellulose, bacteria exit from the "infection tube network".
- ➾Free of cell wall excretions droplets on "infection tubes".
- ➥ Bacterial entry into rudimentary nodule cells (endocytosis,
peribacterial membrane of plant cell membrane origin); symbiosome
- ➾Effect of nodule-specific cystein-rich peptides (NCRs) on terminal differentiation of the symbiosome compartment.
|➾ inhibition of genes regulating bacterial locomotion and division
➾ inhibition/modification of genes coding for bacteroid ribosomal proteins, membrane proteins
change in bacteroid morphology, increase in bacteroid size.
Worth to note that during symbiotic co-operation, endosymbiont efficacy is monitored and regulated by the host plant.
Nodules providing insufficient amounts of nitrogen to the host are
excluded from nutrient exchange i.e. they are deprived from carbon
skeleton (in compound) necessary for life, ultimately
leading to early (controlled) death of the nodule in the soil with
small fraction of bacteria leaving it.
➾ ammonia channels, metabolite/carbohydrate/aminoacid/ion/ transporters are developed. in mutual restructuring,
evolving operative surface for legumerhizobium exchange of substances;
Also, controlled death is the endpoint for nodules of low endosymbiont efficacy when becoming targets for antimicrobial (phenolic) compounds (biotic stress treatment) synthesized and mobilized in the host plant.
The lesson learned from those above is that in symbiosis, in the evolutionary example of plant stress adaptation spanning multitude of generations, it is the root that performs central control in the network of stress responses.
I see that whatever deeper we can get in understanding the finer
mechanisms of biological phenomena still, we always will need the
old-fashioned holistic (overall) approach'
(translation from Hungarian)
In theory, successful
gene transfer of the multigene system described above will serve for the utilization of nitrogen in non-légume plants
deficient in it (e.g. grain/cereal crops).
With the help of computer algorithms, preparation of synthetic multigene systems and artificial DNAs (modular cloning) are already in reality and, separate modules can also be formulated (e.g. expression of -nif- genes coding for the energy-dependent metalloenzyme nitrogenase in ATP synthesizing mitochondria, chloroplasts). However,
in this synthetic approach to evolve atmospheric nitrogen binding in deficient plants, a basic and
unresolved issue is the unique and complex expression control of multigene system components (differential
gene expression). At
this outcome the benefits and responsibilities are to be pondered since,
similar to plants of natural origin the life cycle of plants developed on
synthetic multigene transfer, also ends up in the soil and the
The good news is that the signaling cascade for developing mycorrhizal symbiosis (fungal hyphae assembled on and colonizing host root) can be parallelled with the signaling cascade for developing legumerhizobium (evolutionary preservation).
The excellent technological advantage is that mycorrhizal fungi and rhizobium bacteria both have the ability to synthesize lipochito-oligosaccharide, the signaling substance for chemotactic recognition in the introductory step of symbiosis development (fungal Myc factor, rhizobial Nod factor). Actually, this signaling substance is the acyl-substituted derivative of chitin (chito-oligosaccharide polymer), and chitin is a known trigger of natural immune reactions in plants. Nevertheless, from symbiosis point of view, the acyl-substituted derivative of chitin acts as first-line mediator in stress adaptation.
Rhizobium Nod factor
is indispensable not only in initial partner recognition/selection, but
also in the activation of symbiosis-specific receptors (lysine motif-rich receptor kinases) and postreceptor pathways for the initiation of nodulation in the selected plant.
So, the next step appears to be the harmonization of Myc factor and Nod factor signaling pathways for the opportunity of transferring nitrogen binding capability into nitrogen deficient plants. Having these natural chances together with biotechnology skills,
grain/cereal plants seem to be "educated" for binding atmospheric
nitrogen, since cereal crops too, are characterized by mycorrhizal root colonization.
biotechnology approach targets the diversity of soil dwelling rhizobium
species, the biofilm-forming ability, the slow or rapid growth; all
species involved in nodulation of the host plant (nodulating rhizobia e.g. Bradyrhizobium, Rhizobium,
Mesorhizobium, Sinorhizobium...). In
this approach inter- and intraspecies variations in rhizobia are taken
into consideration from view of symbiotic efficiency (nodulation, nitrogen binding), symbiotic compatibility between host plant and soil bacteria, and symbiotic adaptation to local microenvironment. As a practical consequence of those before, the formulation of rhizobium vaccines and field experiments have begun.
Early in 2017, a meta-analysis including results of 28 international studies (from 1980 to 2016) was published. For test subject and parameters, soybean and soy plant have been selected (crop yield, N-content, host plant nodulation...). It was found that symbiotic efficacy of the local rhizobium populations was exceeded by symbiotic efficacy of rhizobium vaccines (most notably of Bradyrhizobium and Sinorhizobium) formulated experimentally, especially when the amount of rhizobium in the vaccine was decisive (results not unequivocally significant). Enhanced symbiotic efficiency appears to be due to high-density vaccine of heterogeneous populations of rhizobium species.
Also, compared to populations introduced in the vaccine, the meta-analysis has reported an example of local soil-dwelling
rhizobia with higher resilience when adapting to environmental stress stimuli (e.g. adaptation to extreme low or extreme high temperatures).
The efficiency of rhizobium vaccine is influenced by a number of factors including:
genome, All factors require many more further tests.
* microbial competition,
* biotic and abiotic environment,
* soil composition,
* soil physical-chemical characteristics,
* cultivation practice,
* vaccine formulation.
vaccine formulation (25)
- examples for field experiments -
rhizobium species in solution
* surface biofilm on plant seeds (dipping in solution of rhizobia)
* peat mixed solution of rhizobia
* soil mixed solution of rhizobia
* biofilm on glume
at least 109 rhizobia/g
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