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Stress theory inventor Selye, Hans (Selye János: Wien, Österreichisch-Ungarische Monarchie 26 January 1907 - Montréal, Québec, Canada 16 October 1982) was born 111 years ago. Selye's stress theory had earned him worldwide acclaim, led to multitude of disputes and of scientific re-evaluations meanwhile became integral part in next generations' thinking and also in the history of science.
Hans Selye (1936): A Syndrome Produced by Diverse Nocuous Agents Nature 138: p. 32. [Reprint: J. Neuropsychiatry and Clinical Neurosciences (1998) 10: 230a - 231.]
Selye's observations on experimental animals concluded to the recognition of the homeostatic importance (physiological parameters kept at physiological levels in dynamic balanced system) of the HPA axis (the hypothalamo-pituitary-adrenal axis) in regulating stress responses to internal and external stressors. Since the original recognition, overhelming scientific knowledge until now have reached lots of modifications and refinements in the interpretation of Local Adaptation Syndrome (LAS), General Adaptation Syndrome (GAS) and, of the orchestrator-regulator HPA axis. In nowadays' views the phenotypic manifestations of stress responses either controlled or overflown, are driven by homeostatic-allostatic (varying physiological parameters in variable balancing system) regulatory mechanisms. These regulatory mechanisms confined to the neuroimmune-endocrine axis  i.e. the network of overlapping neuronal, endocrine, and immune elements bring about homeostatic-allostatic reactions mediated by signalling molecules (neurotransmitters, cytokines, hormones, secondary-ternary-quaternary messengers, transcription factors, prostanoids, reactive oxygen intermediers...) leading either to stress adaptation or to malformation. 



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 STRESS  ADAPTATION 

OR
Milestones in the interpretation
of
Phylogeny

Comparative Morphological Approach

Linnaeus C. (1735, 1758): 2 evolutionary branches
Plantae,  Animalia 
Binomial nomenclature (genus, species)
Owen R. (1858): 3 evolutionary branches                           Protozoa, Plantae, Animalia
Haeckel E. (1866): 3 evolutionary branches                       Protista, Plantae, Animalia

Pringsheim E. G. (1923): Bacteria branches in                   convergent evolution 

Copeland H.F. (1938):  4 evolutionary branches               Bacteria, Protista, Plantae, Animalia

Chatton E. (1938):  2 evolutionary branches                       Procaryotae, Eucaryotae


Phylogenetic - Phylogenomic - Molecular (RNAs, Proteins, Lipids) Comparative Approach

Zuckerkandl E. & Pauling L. (1965)
Semantophoretic molecules 
(information carriers: genes, RNAs, proteins) 
Episemantic molecules             (enzyme-catalyzed template-free syntheses)
Asemantic molecules 
Stanier R. Y. (1971)
Divergence of Procaryotae at the beginning 
of cellular evolution
Whittaker R.H. (1978):  5 kingdoms                               Animalia, Plantae, Fungi, Protista, Monera 
 wherein 
Monera= Eubacteria + Archeobacteria
Woese C.R. et al. (1990): 3 domain system
Bacteria, Archaea, Eucarya
comprising 6 kingdoms 
Grosch E.G. & Hazen R.M. (2015)
Geosphere and Microbiosphere in coevolution
Kang Liu et al. (2017)
Plant Taxonomy based on comparative analyses of primary and secondary metabolites
Sourabh Jain et al. (2017)
New Order: Megavirales  
(genome size 100-2550 kB)
acquisition and exchange of genes in environmental interactions


Source:
Zuckerkandl E. & Pauling L. (1965): Molecules as Documents of Evolutionary History
J. Theoret. Biol. 8: 357-366.
Whittaker R.H. (1969): New Concepts of Kingdoms of Organisms  
Science 163: 150-160. 
Woese C. R. Kandler O. & Wheelis M.L. (1990): Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya
Proc. Natl. Acad. Sci. USA 87: 4576-4579.
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
Sourabh Jain et al. (2017):  MimiLook: A Phylogenetic Workflow for Detection of Gene Acquisition in Major Orthologous Groups of Megavirales
Viruses  9(4): 72  doi:10.3390/v9040072
Stress adaptation

Similar 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/major-minor genes; the problem of genetic determination; mechanisms of cellular proteostasis and metabolic adaptation; intracellular redox systems).

How is it with Plant Kingdom?

 
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.


Elements in Plant Defense and Immunity 

A/  Structural
B/  Induced

The evolutionary example of plant stress adaptation spanning multitude of generations is symbiosis (1-29). 

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 followers (1990s years) extend the interpretation therefore, the term symbiosis covers the coexistence of all organic forms (living organisms, viruses, viroids, plasmids...) 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 disadvantages (parasitism, commensalism, 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,
  • determined 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.


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Barter in Plant Kingdom
or,
Symbiotic Processes
with 
Application


Suggested online book for navigation in Plant Physiology:

Ördög Vince, Molnár Zoltán: Plant Physiology, 2011  
 online study text for MSc students at the faculty of Agriculture     
Hungary

If Search by Keywords:  

Plant Physiology  
(Journal of the American Society of Plant Biologists)





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

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, Sinorhizobium) 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.

G-24 

THE  PROCESS  (1,5,8-11,14-21,28,29)

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 and adhesion. 
The {légume ➾ rhizobium ➥} 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 genes. 
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 N2 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.
Nevertheless, 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 (➥Sinorhizobium meliloti)
  • ➾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 factor (chitin-based 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 is formed. 
  • ➾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.
➾ peribacteroid membrane
and  
➥ bacterial surface
in mutual restructuring,
evolving operative surface for legumerhizobium exchange of substances;
➾ ammonia channels, metabolite/carbohydrate/aminoacid/ion/ transporters are developed.


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.
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.


 G-25

APPLICATION? (17,23,25,27,29)

'However, 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'            Hans Selye              (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 consumer fauna. 

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. 

Biodiversity-based 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:

* microbial genome, 
* microbial competition, 
* biotic and abiotic environment,  
* climate, 
* soil composition, 
* soil physical-chemical characteristics, 
* cultivation practice, 
* vaccine formulation.

All factors require many more further tests.

Rhizobium vaccine formulation (25)
- examples for field experiments -
basis: 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             

Source

1. Nap J-P., Bisseling T.(1990): Developmental Bology of a Plant-Prokaryote Symbiosis: The Legume Root Nodule   Science 250:  948-954.
2. Daida J.M., Grasso C.S., Stanhope S.A., Ross S.J.(1996): Symbionticism and Complex Adaptive Systems I: Implications of Having Symbiosis Occur in Nature    Evolutionary Programming V,: Proceedings of the Fifth Annual Conference on Evolutionary Programming   Cambridge MA, The MIT Press pp. 1-10.
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5.  Jones K.M., Kobayashi H., Davies B.W., Taga M.E., Walker G.C.(2007): How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model     Nat. Rev. Microbiol.  5:  619–633.
6. Reape T.J., Molony E.M., McCabe P.F.(2008): Programmed cell death in plants: distinguishing between different modes    J. Exp. Bot.  59:  435-444.
7. Rodriguez R., Redman R.(2008): More than 400 million years of evolution and some plants still can't make it on their own: plant stress tolerance via fungal symbiosis    J. Exp. Bot. 59: 1109-1114.
8.  Hernández G,. Valdés-López O., Ramírez M., Goffard N., Weiller G., Aparicio-Fabre R., Fuentes S. I., Erban A., Kopka J.,  Udvardi M.K., Vance C.P. (2009): Global Changes in the Transcript and Metabolic Profiles during Symbiotic Nitrogen Fixation in Phosphorus-Stressed Common Bean Plants    Plant Physiology  151: 1221–1238.    PMCID: PMC2773089
9.  Van de Velde W. et al (+19) (2010): Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis      Science 327: 1122-1126.
10.  Wang D., Griffitts J., Starker C., Fedorova E., Limpens E., Ivanov S., Bisseling T., Long S.(2010):  A Nodule-Specific Protein Secretory Pathway Required for Nitrogen-Fixing Symbiosis    Science  327: 1126-1129.
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12. Behie S.W., Zelisko P.M., Bidochka M.J.(2012): Endophytic Insect-Parasitic Fungi Translocate Nitrogen Directly from Insects to Plants    Science 336: 1576-1577.
13. Kivlin S.N., Emery S.M., Rudgers J.A.(2013): Fungal symbionts alter plant responses to global change     Am. J. Bot. 100: 1445-1457.
14. Haag A.F., Arnold M.F.F., Myka K.K., Kerscher B., Dall'Angelo S., Zanda M., Mergaert P., Ferguson G.P.(2013): Molecular insights into bacteroid development during Rhizobium–legume symbiosis   FEMS Microbiol. Rev. 37: 364-383.
15. Liang Y., Tóth K., Cao Y., Tanaka K., Espinoza C., Stacey G. (2014): Lipochitooligosaccharide recognition: an ancient story   New Phytologist 204: 289–296.
16. Ying Caoa, En-Tao Wangb, Liang Zhaoa, Wei-Min Chena, Ge-Hong Weia(2014): Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China     Soil Biology and Biochemistry 78: 128–137.
17. Oldroyd G.E.D., Dixon R.(2014): Biotechnological solutions to the nitrogen problem    Current Opinion in Biotechnology 26:  19-24.
18. Djordjevic M.A., Mohd-Radzman M.A., Imin N.(2015): Small-peptide signals that control root nodule number, development, and symbiosis      J. Exp. Bot. 66 : 5171-5181.
19. Delaux P-M., Radhakrishnan G., Oldroyd G.(2015): Tracing the evolutionary path to nitrogen-fixing crops  Current Opinion in Plant Biology  26: 95–99.
20. Stec N., Banasiak J., Jasiński M.(2016): Abscisic acid - an overlooked player in plant-microbe symbioses formation? Acta Biochimica Polonica, 63: 53-58.
21. Verma V., Ravindran P., Kumar P.P.(2016): Plant hormone-mediated regulation of stress responses    BMC Plant Biology  16: 86  DOI: 10.1186/s12870-016-0771-y
22. Bhagya Iyera, Mahendrapal Singh Rajputa, Rahul Joga, b, Ekta Joshia, Krishna Bharwada, Shalini Rajkumar (2016): Organic acid mediated repression of sugar utilization in rhizobia    Microbiological Research 192: 211–220.
23. Mus F. et al (+13) (2016): Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes   Appl. Environ. Microbiol. 82: 3698-3710.
24. Behie S.W., Moreira C.C., Sementchoukova I., Barelli L., Zelisko P.M., Bidochka M.J.(2017): Carbon translocation from a plant to an insect-pathogenic endophytic fungus    Nature Communications 8: Article number: 14245
25. Thilakarathna M.S., Raizada M.N. (2017):  A meta-analysis of the effectiveness of diverse rhizobia inoculants on soybean traits under field conditions     Soil Biology and Biochemistry  105: 177–196.
26. Zhao Jun Jia, Hui Yanb, Qing Guo Cuie, En Tao Wangb, Wen Feng Chenb, Wen Xin Chen(2017):  Competition between rhizobia under different environmental conditions affects the nodulation of a legume   Systematic and Applied Microbiology  40: 114–119.
27. Nitroplast: A light-driven, synthetic nitrogen-fixing organelle (Rosser Laboratory ongoing project)
28. Wright G.S.A. et al (+ 13) (2018): Architecture of the complete oxygen-sensing FixL-FixJ two-component signal transduction system   Sci. Signal. 11: Issue 525, eaaq0825
29. Kereszt A., Mergaert P., Montiel J., Endre G., Kondorosi É. (2018): Impact of Plant Peptides on Symbiotic Nodule Development and Functioning    Front Plant Sci. 2018 Jul 17;9:1026. doi: 10.3389/fpls.2018.01026.


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