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Sustainable Agriculture Reviews 45

Praveen Guleria
Vineet Kumar
Eric Lichtfouse Editors

Sustainable
Agriculture
Reviews 45
Legume Agriculture and Biotechnology
Vol 1
Sustainable Agriculture Reviews

Volume 45

Series Editor
Eric Lichtfouse
CNRS, IRD, INRAE, Coll France, CEREGE, Aix-Marseille University,
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Sustainable agriculture is a rapidly growing field aiming at producing food and

energy in a sustainable way for humans and their children. Sustainable agriculture
is a discipline that addresses current issues such as climate change, increasing food
and fuel prices, poor-nation starvation, rich-nation obesity, water pollution, soil
erosion, fertility loss, pest control, and biodiversity depletion.
Novel, environmentally-friendly solutions are proposed based on integrated
knowledge from sciences as diverse as agronomy, soil science, molecular biology,
chemistry, toxicology, ecology, economy, and social sciences. Indeed, sustainable
agriculture decipher mechanisms of processes that occur from the molecular level
to the farming system to the global level at time scales ranging from seconds to
centuries. For that, scientists use the system approach that involves studying
components and interactions of a whole system to address scientific, economic and
social issues. In that respect, sustainable agriculture is not a classical, narrow
science. Instead of solving problems using the classical painkiller approach that
treats only negative impacts, sustainable agriculture treats problem sources.
Because most actual society issues are now intertwined, global, and fast-
developing, sustainable agriculture will bring solutions to build a safer world. This
book series gathers review articles that analyze current agricultural issues and
knowledge, then propose alternative solutions. It will therefore help all scientists,
decision-makers, professors, farmers and politicians who wish to build a safe
agriculture, energy and food system for future generations.

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Praveen Guleria • Vineet Kumar
Eric Lichtfouse
Editors

Sustainable Agriculture
Reviews 45
Legume Agriculture and Biotechnology Vol 1
Editors
Praveen Guleria Vineet Kumar
Plant Biotechnology and Genetic Department of Biotechnology, School of
Engineering Lab, Department of Bioengineering and Biosciences
Biotechnology Lovely Professional University
DAV University Phagwara, India
Jalandhar, Punjab, India

Eric Lichtfouse
CNRS, IRD, INRAE, Coll
France, CEREGE
Aix-Marseille University
Aix-en-Provence, France

ISSN 2210-4410     ISSN 2210-4429 (electronic)

Sustainable Agriculture Reviews
ISBN 978-3-030-53016-7    ISBN 978-3-030-53017-4 (eBook)
https://doi.org/10.1007/978-3-030-53017-4

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature
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Preface

On January 30, 1988, my twenty-seventh birthday, I became a strict vegetarian. I

developed a passion for health and nutrition. My diet consists of fruits, vegetables,
grains, nuts and legumes only, and has for the past 15 years now. – Dexter
Scott King.
Legumes are an important constituent of vegetarian diet across the globe.
Legumes have been considered of great significance in counteracting malnutrition
problems because of their high protein content and easy starch digestibility. Recent
years have witnessed advancement in legume cultivation research and biotechnol-
ogy owing to their potential health benefits. The bioactive and antioxidant-rich

v
vi Preface

nature of legumes is responsible for health benefits associated with them. Legumes
contain micro- and macronutrients of direct human benefits. Further, legumes are a
rich source of polyphenolic phytochemicals, phenolic acids, flavonoids and tannins.
These polyphenols have a significant role in several physiological and metabolic
processes. They are an important source of natural dietary antioxidants that act as
free radical scavengers, reducing agents, chelating agents of pro-oxidant metals and
quenchers of the formation of singlet oxygen, which allow them to protect cells
against oxidative damage. Majority of polyphenols are present in legume seeds,
primarily in the seed coat. Further, the accumulation of polyphenols and antioxidant
bioactive compounds has been regulated by various seed-processing methods
including dehulling, germination, roasting and pressure boiling. These methods sig-
nificantly increase the antioxidant potential of legume seeds. Research on legume
crops has gained specific interest due to its unexploited potential to eradicate protein
energy malnutrition. Targeting the accumulation of legume bioactive compounds
using various biotechnological approaches and exploring their probable therapeutic
potential in context to various human diseases is of utmost need and importance.
This book, entitled Legume Agriculture and Biotechnology, published in the
series Sustainable Agriculture Reviews, is written by 10 international contributors
from 5 countries. The chapters review bioactive compounds and their applications,
conventional breeding, and biotechnology-based methods for legume sustainability
and nutritional enhancement.
The first chapter by Lahiri et al. summarises an introductory aspect of legumes
towards biotechnology with focus on nitrogen fixation and their bioactive compo-
sition. The second chapter by Tiwari et al. provides an overview of the applica-
tions of bioactive peptides derived from legumes in food and healthcare industries.
In Chap. 3, Budhwar and Chakraborty describe the comparative analysis of nutri-
ent as well as anti-nutrient components of legumes along with their nutraceutical
properties. Singh et al. discuss in Chap. 4 the antioxidant components of legumes
and the impact of processing ways on antioxidant compounds as well as their
activities. Lavudi and Suthari describe legume seed galactomannans and their
multipurpose applications in Chap. 5, and Guaadaoui et al. discuss the medicinal
application and nutraceuticals properties of the diverse bioactive compounds of
legumes in Chap. 6. Feki et al. in Chap. 7 provide an overview of underlying
molecular mechanism behind the symbiotic association between legumes and rhi-
zobia, and Muthini et al. in Chap. 8 describe the benefits of rhizobia and other
plant growth–promoting microorganisms for sustainable improvement of legume
production in small agroecosystems. In Chap. 9, Khare and Chauhan provide new
insight in the development and application of new plant breeding techniques to
benefit human health and maintain cost effectiveness. The final chapter by
Mangena summarises challenges faced during soybean genetic improvement, the
vulnerability against drought stress and approaches to improve soybean growth
and productivity.
The editors are thankful to all the authors who contributed to this book for their
efforts in producing timely and high-quality chapters. The creation of this book
Preface vii

would not have been possible without the assistance of several colleagues and
friends. They have helped by choosing contributors, reviewing chapters and in many
other ways. Finally, we would like to thank the staff of Springer Nature for copy-
editing this book in a highly professional manner.

Jalandhar, Punjab, India Praveen Guleria

Phagwara, India Vineet Kumar
Aix-en-Provence FranceEric Lichtfouse
Contents

1 An Introduction to Legume Biotechnology ������������������������������������������    1

Dibyajit Lahiri, Moupriya Nag, Amrita Jasu, Bandita Dutta,
Ritwik Banerjee, Dipro Mukherjee, Sayantani Garai,
and Rina Rani Ray
2 Legume Derived Bioactive Peptides ������������������������������������������������������   29
Pragya Tiwari, Anjani Devi Chintagunta, Vijaya R. Dirisala,
and N. S. Sampath Kumar
3 Novel Dietary and Nutraceutical Supplements from Legumes ����������   53
Savita Budhwar and Manali Chakraborty
4 Antioxidant Profile of Legume Seeds ����������������������������������������������������   71
Balwinder Singh, Jatinder Pal Singh, Amarbir Kaur,
Amritpal Kaur, and Narpinder Singh
5 Application of Legume Seed Galactomannan Polysaccharides ����������   97
Harikrishna Naik Lavudi and Sateesh Suthari
6 Legumes as Preventive Nutraceuticals for Chronic Diseases�������������� 115
Abdelkarim Guaadaoui, Meryem Elyadini,
and Abdellah Hamal
7 Legume Symbiotic Interaction from Gene to Whole Plant������������������ 137
Kaouthar Feki, Faiçal Brini, Moncef Mrabet,
and Haythem Mhadhbi
8 Optimizing Rhizobium-Legume Symbiosis
in Smallholder Agroecosystems�������������������������������������������������������������� 159
Morris Muthini, Richard Awino, Kibet Charles Kirui,
Kipkorir Koech, Abdul A. Jalloh, and Ezekiel Mugendi Njeru

ix
x Contents

9 Transformation of Agricultural Breeding Techniques

Using Biotechnology as a Tool���������������������������������������������������������������� 179
Ekta Khare and Pallavi Singh Chauhan
10 Genetic Transformation to Confer Drought Stress
Tolerance in Soybean (Glycine max L.)�������������������������������������������������� 193
Phetole Mangena

Index������������������������������������������������������������������������������������������������������������������ 225
About the Editors

Praveen Guleria is Assistant Professor in the Department of Biotechnology at

DAV University, Jalandhar, Punjab, India. She has worked in the areas of Plant
Biotechnology, Plant Metabolic Engineering, and Plant Stress Biology at CSIR –
Institute of Himalayan Bioresource Technology, Palampur, HP, India.
Her research interests include plant stress biology, plant small RNA biology,
plant epigenomics, and nanotoxicity. She has published several research articles
in various peer-reviewed journals. She also serves as the editorial board member
and reviewer for certain international peer-reviewed journals. She has been
awarded the SERB Start Up Grant by DST, GOI. She has also been awarded the
prestigious “Bharat Gaurav Award” by the India International Friendship Society,
New Delhi. She has also received various awards like CSIR/ICMR – junior
research fellowship, CSIR – senior research fellowship, and state level merit
scholarship awards.

xi
xii About the Editors

Vineet Kumar is Assistant Professor in the Department of Biotechnology, Lovely

Professional University, Jalandhar, Punjab, India. He has worked in different areas
of biotechnology and nanotechnology in various institutes and universities in India,
namely, Panjab University Chandigarh; CSIR –Institute of Microbial Technology,
Chandigarh, India; and CSIR – Institute of Himalayan Bioresource Technology and
Himachal Pradesh University. He has published many articles in these areas featur-
ing in peer-reviewed journals. He also serves as editorial board member and reviewer
for international peer-reviewed journals. He has received various awards like Dr
DSK-postdoctoral fellowship, senior research fellowship, and best poster awards.

Eric Lichtfouse is a biogeochemist at Aix-Marseille University who has invented

carbon-13 dating, a molecular-level method allowing to study the dynamics of
organic compounds in temporal pools of complex environmental media. He is Chief
Editor of the journal Environmental Chemistry Letters, and the book series
Sustainable Agriculture Reviews and Environmental Chemistry for a Sustainable
World. He is the author of the book Scientific Writing for Impact Factor Journals,
which includes an innovative writing tool: the Micro-Article.
Contributors

Richard Awino Department of Biochemistry, Microbiology and Biotechnology,

Kenyatta University, Nairobi, Kenya
Ritwik Banerjee Department of Biotechnology, University of Engineering &
Management, Kolkata, India
Faiçal Brini Biotechnology and Plant Improvement Laboratory, Center of
Biotechnology of Sfax (CBS), University of Sfax, Sfax, Tunisia
Savita Budhwar Department of Nutrition Biology, Central University of Haryana,
Mahendergarh, Jant-Pali, Haryana, India
Manali Chakraborty Department of Nutrition Biology, Central University of
Haryana, Mahendergarh, Jant-Pali, Haryana, India
Pallavi Singh Chauhan Department of Life Sciences, I.T.M. University, Gwalior,
Madhya Pradesh, India
Anjani Devi Chintagunta Department of Biotechnology, Vignan’s Foundation for
Science, Technology and Research, Guntur, Andhra Pradesh, India
Vijaya R. Dirisala Department of Biotechnology, Vignan’s Foundation for
Science, Technology and Research, Guntur, Andhra Pradesh, India
Bandita Dutta Department of Biotechnology, Maulana Abul Kalam Azad
University of Technology, Kolkata, West Bengal, India
Meryem Elyadini Laboratory of Biochemistry, Environment and Agrifood,
Department of Biology, Faculty of Sciences and technology – Mohammedia,
Hassan the Second University, Mohammedia, Morocco
Kaouthar Feki Laboratory of Legumes, Center of Biotechnology of Borj-Cédria,
Hammam Lif, Tunisia
Sayantani Garai Department of Biotechnology, University of Engineering &
Management, Kolkata, India

xiii
xiv Contributors

Abdelkarim Guaadaoui Laboratory of Physiology, Genetic and

Ethnopharmacology (LPGE), Department of Biology, Faculty of Sciences – Oujda
(FSO), Mohammed the First University (UMP), Oujda, Morocco
Abdellah Hamal Laboratory of Physiology, Genetic and Ethnopharmacology
(LPGE), Department of Biology, Faculty of Sciences – Oujda (FSO), Mohammed
the First University (UMP), Oujda, Morocco
Abdul A. Jalloh Department of Biochemistry, Microbiology and Biotechnology,
Kenyatta University, Nairobi, Kenya
Amrita Jasu Department of Biotechnology, Maulana Abul Kalam Azad University
of Technology, Kolkata, West Bengal, India
Amarbir Kaur Department of Food Science and Technology, Guru Nanak Dev
University, Amritsar, Punjab, India
Amritpal Kaur Department of Food Science and Technology, Guru Nanak Dev
University, Amritsar, Punjab, India
Ekta Khare Department of Pharmacy, I.T.M. University, Gwalior, Madhya
Pradesh, India
Kibet Charles Kirui Department of Biochemistry, Microbiology and
Biotechnology, Kenyatta University, Nairobi, Kenya
Kipkorir Koech Department of Biochemistry, Microbiology and Biotechnology,
Kenyatta University, Nairobi, Kenya
N. S. Sampath Kumar Department of Biotechnology, Vignan’s Foundation for
Science, Technology and Research, Guntur, Andhra Pradesh, India
Dibyajit Lahiri Department of Biotechnology, University of Engineering &
Management, Kolkata, India
Harikrishna Naik Lavudi Department of Plant Sciences, University of Hyderabad,
Hyderabad, Telangana, India
Phetole Mangena Department of Biodiversity, School of Molecular and Life
Sciences, Faculty of Science and Agriculture, University of Limpopo, Sovenga,
South Africa
Haythem Mhadhbi Laboratory of Legumes, Center of Biotechnology of Borj-­
Cédria, Hammam Lif, Tunisia
Moncef Mrabet Laboratory of Legumes, Center of Biotechnology of Borj-Cédria,
Hammam Lif, Tunisia
Dipro Mukherjee Department of Biotechnology, University of Engineering &
Management, Kolkata, India
Morris Muthini Department of Biochemistry, Microbiology and Biotechnology,
Kenyatta University, Nairobi, Kenya
Contributors xv

Moupriya Nag Department of Biotechnology, University of Engineering &

Management, Kolkata, India
Ezekiel Mugendi Njeru Department of Biochemistry, Microbiology and
Biotechnology, Kenyatta University, Nairobi, Kenya
Rina Rani Ray Department of Biotechnology, Maulana Abul Kalam Azad
University of Technology, Kolkata, West Bengal, India
Balwinder Singh Department of Biotechnology, Khalsa College, Amritsar,
Punjab, India
Jatinder Pal Singh Department of Food Science and Technology, Guru Nanak
Dev University, Amritsar, Punjab, India
Narpinder Singh Department of Food Science and Technology, Guru Nanak Dev
University, Amritsar, Punjab, India
Sateesh Suthari Department of Plant Sciences, University of Hyderabad,
Hyderabad, Telangana, India
Department of Botany, Vaagdevi Degree & PG College, Warangal, Telangana, India
Pragya Tiwari Molecular Metabolic Engineering Laboratory, Department of
Biotechnology, Yeungnam University, Gyeongsan, Gyeongbuk, Republic of Korea
Chapter 1
An Introduction to Legume Biotechnology

Dibyajit Lahiri, Moupriya Nag, Amrita Jasu, Bandita Dutta,

Ritwik Banerjee, Dipro Mukherjee, Sayantani Garai, and Rina Rani Ray

Abstract Legumes are the group of predominant nitrogen fixers that act as a source
of wide variety of secondary metabolites that act as a line of defence against various
bacterial, fungal, parasitic and predatory species. The symbiotic bacterial species
establishes a syntopic interaction by quorum sensing and develop a biofilm that help
is building up of the symbiotic relation with the plant. This association not only
helps in the mode of nitrogen fixation but also helps in increasing the bioactive
contents along with various types of abiotic components found in soil. These bioac-
tive compounds have wide therapeutic potential, as significantly used as anti-aging,
antimicrobial, antibiofilm, antioxidant, antidiabetic, anti-inflammatory and cardio-
protective agents. The compounds also act as antiangiogenic agent and prevent the
proliferation of disease causing pathogens. Hence, legumes not only help in sustain-
able development of plant and agriculture, but also possess significant therapeutic
potential to promote human health. The present article thus reviews the contribution
of legumes towards nitrogen fixation to facilitate plant growth and discusses their
bioactive compounds having beneficial role in regulating human health.

Keywords Legumes · Secondary metabolites · Bioactive · Therapeutic · Nitrogen

fixation · Antimicrobial · Antioxidant · Stress

Abbreviations

AMF Arbuscular mycorrhizal fungi

CHS Chalcone synthase
IFR Isoflavone reductase
IRS Induced response system

Authors Dibyajit Lahiri, Moupriya Nag, Amrita Jasu have equally contributed to this chapter.

D. Lahiri · M. Nag · R. Banerjee · D. Mukherjee · S. Garai

Department of Biotechnology, University of Engineering & Management, Kolkata, India
A. Jasu · B. Dutta · R. R. Ray (*)
Department of Biotechnology, Maulana Abul Kalam Azad University of Technology,
Kolkata, West Bengal, India

© The Editor(s) (if applicable) and The Author(s), under exclusive license to 1
Springer Nature Switzerland AG 2020
P. Guleria et al. (eds.), Sustainable Agriculture Reviews 45, Sustainable
Agriculture Reviews 45, https://doi.org/10.1007/978-3-030-53017-4_1
2 D. Lahiri et al.

PAL Phenylalanine ammonia lyase

PAPPP Proline-associated pentose phosphate pathway
ROS Reactive oxygen species
SAR System acquired response

1.1 Introduction

There is a chance of severe food scarcity in coming era as the population increases
at a geometric progression and the food productivity increases at arithmetic pro-
gression. Researches forecast that the population of the world will reach almost to
9.6 billion by 2050. Therefore there is a substantial increase in dietary intake of
legumes as replacement of cereal grains (Venn and Mann 2004) and the legumes
serve as one of the important sources of food to a large population. They not only
act as the richest source of proteins but also are the reservoirs of large number of
bioactive compounds that in turn act as important food supplement for the human
population and livestock. They also contain a large number of trace elements like
magnesium, potassium, calcium, iron, zinc, copper and manganese (Stagnari et al.
2017) which are of immense importance for human metabolism. A significant quan-
tity of vitamins, minerals, carbohydrates, fibres and energy (Frankel 1996) can be
obtained from legumes.
Legumes in association with the endophytic and epiphytic bacteria like Rhizobium
leguminosarum or Clostridium acetobutylicum, developing biofilm on their root
surface help in maintaining as well as enhancing the nitrogenous adequacy of the
soil. As a result, they are used as an important component during crop rotation in
agriculture. Common examples of legumes include pulses, beans, lentils, peas, soya
beans, peanuts, tamarind, etc. (Harborne 1973; Mackeen et al. 1997).
The major active compounds present in legumes comprise of polyphenols and
flavonoids which impart significant antioxidant potential to them. These phytocom-
pounds scavenge the free oxygen species and protect the cells from damage (Frankel
1996). Hence natural antioxidant phytochemicals extracted from legumes play an
indispensable role for human health targeting various health disorders like cardio-
vascular disease, tumorous growth or ischemic diseases (Ito et al. 1983). Other
active compounds including glycosides, tannins, saponins and alkaloids play a sig-
nificant role in maintaining human health (Flight Clifton 2006; Huda-Faujan et al.
2009). It is well documented that these active ingredients actually help in protecting
plants against various biotic and abiotic stresses (Ngoci et al. 2011).
The present chapter predominantly focuses on various types of bioactive com-
pounds present in legumes, factors influencing their biosynthesis and their signifi-
cant applications (Fig. 1.1).
1 An Introduction to Legume Biotechnology 3

Fig. 1.1 Mutualistic relation between legumes and nitrogen fixing bacteria

1.1.1 Plant Legumes: History

Leguminosae is one of the important member of plant family which nearly comprises
of 800 different types of genera and about 20,000 species and is the third largest fam-
ily of flowering plants. Legumes or beans were one of the first domesticated plants
which appeared before 6000 B.C. Now-a-days, there has been a high demand for
nutritive foods, not only in the scientific community but also in the economic and
social aspect of living. According to The United Nations, 2016 has been declared as
the International Year of Pulses, recognizing pulse cultivation beneficial for the sus-
tainable nitrogen enrichment of agricultural soil and their nutritive impact on
human health.
The American 2015 Dietary Guidelines henceforth recommended pulses’ con-
sumption as “Sustainable Diets” and a high intake of legumes (beans), is linked to
significantly lower risks of heart disease, high blood pressure, stroke, and type 2
diabetes, hyperlipidaemia and causes weight management (Polak et al. 2015).
With diversified dietary habits worldwide, a balanced diet chart must be main-
tained to reach optimum nutritional value, as like:
1. Utilization of dietary component for the purpose of providing energy;
2. Biochemical food components to maintain the regulatory functions.
4 D. Lahiri et al.

Therefore, it is very important to have a set of balanced nutrients within the diet
(Nishida et al. 2004). The FAO-WHO Group of Experts established the following
dietary recommendations:
• 60% carbohydrates
• 3% fibre
• protein at an amount so that total calorie intake must be below 15%
• lipids not more than 25%; comprising 75% of plant foods and 25% derived from
animal sources

1.2 Roles of Legumes in Agriculture

1.2.1 Rhizobium-Legume Symbiosis

The nitrogen starvation in the surrounding environment results in the development

of symbiotic association between the rhizobial microbiota and the legumes (Jensen
et al. 2012). This interaction by cellular signalling results in the development of root
nodules which provides a predominant site for the conversion of the bacterial spe-
cies to nitrogen fixing bacteriods. The mutualistic relation is established by the tak-
ing up of the nitrogenous compounds fixed by the bacteriods and the utilization of
assimilated carbon from the plants by the bacterial species (MarÃti and Kondorosi
2014). The two predominant groups of bacterial cells that participate in the mecha-
nism of nitrogen fixation are classified into two categories, namely α-proteobacteria
and β-proteobacteria, collectively termed as Rhizobia (Chen et al. 2003; MacLean
et al. 2007).
Wide range of gram positive Rhizobiaceae like bacterial species is known that
help in establishing a mutualistic relationship with legumes for nitrogen fixation.
These legumes develop a rhizome which are deep enough and allows to establish
strong symbiotic interaction with the Rhizobiaceae (Gram-negative bacteria). It has
a potent nutritive value for livestock farming systems, the use of nitrogenous fertil-
izers are reduced maximally due to the use of the forage legumes. This symbiotic
relationship reduce atmospheric Nitrogen to Ammonia which later gets converted
into amino acids for the synthesis of proteins in plants.
Nodule formation can be on various plant parts including stems and roots and
they can be indeterminate with apical meristematic growth (Martin and Liras 1989).
The process of conversion of atmospheric nitrogen to useful nitrogenous com-
pounds is usually carried out by rhizobium bacteroids in which several parts of both
partner organisms are involved. This mechanism is enunciated by the use leghaemo-
globin, which helps in removing the oxygen from the symbiosomes by the nitroge-
nase enzyme, predominantly available within the bacteroids having microaerophilic
environment. The pink colour in the nodule region provides the distinct expression
on the above mentioned circumstances, which ultimately indicates an effective
establishment of symbiotic relationship (Elexsona et al. 2014).
1 An Introduction to Legume Biotechnology 5

1.2.2 Symbiotic Nitrogen Fixation

Atmospheric Nitrogen, although considered to be an inert gas, is one of the essential

elements that are required for survival. But most of the organisms are capable of
utilizing ammonia (NH3), rather than the inert N2 to synthesize nucleic acids, amino
acids, proteins and other nitrogen-containing components necessary for life.
Hence, the mechanism of fixation of atmospheric nitrogen is of utter importance
to convert inert N2 into biologically useful NH3 (the only form that is utilized by all
organisms) which is naturally mediated only by Nitrogen fixing Rhizobiaceae
(α-Proteobacteria) (Sørensen and Sessitsch 2007). Nitrogen fixing bacteria is ben-
eficial for when other plants has to release nitrogen to the environment after their
death, few bacteria lives clubbed with the plant as in legumes and a few other plants
where they live in small bulgings on the roots forming nodules. Within these nod-
ules, upon nitrogen fixation they produce NH3 that is henceforth absorbed by the
plant. Thus, nitrogen fixation by legumes stands out as an important relationship
between a plant and the bacteria.
There are many forms of biological nitrogen fixation in nature; with the help of
lichens, blue-green algae and various soil bacteria in association with the plants.
The natural ecosystem gets enriched by the significant quantities of NH3 due to the
amount of nitrogen fixed, which can be in the range of 25–75 lb of nitrogen/acre/
year in a natural ecosystem to several hundred pounds in a cropping system (Burton
1972; Guldan et al. 1996; Frankow-Lindberg and Dahlin 2013).
Formation of root nodules marks the initiation of nitrogen fixation. The rhizo-
spheric bacterium invades the root, multiplies within its cortex cells and gets sup-
plied with all the necessary nutrients for its multiplication. Within a week or two
following the infection, small nodules start to get visible with naked eye. When
nodules are young, usually white or grey inside, are unable to fix nitrogen. As they
gradually grow in size, they turn pink or reddish in colour, indicating the initiation
of nitrogen fixation. The appearance of pink or red colour is due to the leghemoglo-
bin (as similar to the hemoglobin present in blood) that controls by restricting the
oxygen flow to the bacteria, creating an anaerobic environment.

1.2.3  eguminous Flavonoid and Bacterial Nod (Nodulation)

L
Gene Expression During Nitrogen Fixation

Flavonoid compounds are secreted during nitrogen limiting conditions into the rhi-
zosphere. These flavonoids induce the expression of nod genes by activating the
NodD proteins, LysR type transcription regulators (Long 1996). The synthesis of
Nod factor or the nod gene expression initiates after the binding of NodD protein
into the nod boxes (a conserved DNA motif) present in the upstream of the Nod
operons (Fisher et al. 1998; Rostas et al. 1986).
6 D. Lahiri et al.

Nod factor is an essential lipo-chito-oligosaccharide signal for the initiation of

symbiotic relationship. This factor has first adapted themselves to recognize different
leguminous flavonoids and the symbiotic relationship takes place only after establish-
ing the recognition specificity. Therefore those flavonoids are called “infection flavo-
noids” due to their high accumulation in the infection site and increased biosynthesis
after the infection by the pre recognized rhizobia. The first flavonoid identified was
luteolin which has broad range of rhizobial strain specificity (Liu and Murray 2016).
Thereafter Nod factors directly bind to the LysM domain of the Nod factor recep-
tors (e.g. NFR1, NFR2 etc.) and facilitate the activation of downstream signalling
(Limpens et al. 2003). This Nod factor recognition specifically determines host
range in the species level. Hence the leguminous bioactive compounds such as fla-
vonoids play a crucial role in rhizobium-legume symbiosis.

1.3 Bioactive Compounds Present Within Legumes

Legumes are widely grown for the large number of beneficial compounds being pres-
ent within them. The nutritional contents vary from proteins, fibres, minerals, starch
and vitamins. It also contains a large amount of phytocompounds. These major group
of secondary metabolites comprises of alkaloids, peptides, cyanogens, polyketides,
simple phenolics like flavonoids (which mainly contain phytoestrogens and cate-
chins), sterols, polyphenols, saponins, phytates and terpenoid (Tables 1.1 and 1.2)
(Harborne and Turner 1984; Hegnauer and Hegnauer 1994; Kinghorn and Balandrin
1984; Seigler 1998; Southon 1994; Wink 1993b; Veitch 2010). The legumes also play
an important role as nutraceuticals as they contain bioactive peptides which have an
important role in human welfare. The bioactive compounds present in legumes pos-
sess antioxidant, hypocholesterolemic, antithrombotic and antioxidant activities. It
has been analysed that flavonoids obtained from these legumes has anticancer activi-
ties. Legumes also contain large quantities of hydrophilic phytochemicals like ascor-
bic acid, polyphenols and phenolic acids which help in the redemption of cancer risk
and also act as immunostimulants. This diversification also encircles in modifying
lipophilic compounds like tocopherols and carotenoids which help in preventing car-
diovascular diseases. The advancement in the field of ethnopharmacology in last few
decades has provided us with the concept of large number of active molecules which
has a sincere role in inhibiting the microbial proliferations.
Research is still going on to elucidate human health regulatory bioactive com-
pounds present within the legumes (Hegnauer and Hegnauer 1994; Southon 1994).
Majority of the identified bioactive compounds has pharmacological and toxico-
logical activities (Wink et al. 1998; reviewed in Teuscher and Lindequist 2010).
Many of the alkaloids are either neurotoxins or neuromodulators (reviewed in Wink
1992, 1993a, 2000, 2007; Wink and Schimmer 2010). Plants specifically use these
compounds for protection against herbivores as well as various microbial infections
(McLean 1970; Hartmann and Witte 1995; Wink and Schimmer 2010).
1 An Introduction to Legume Biotechnology 7

Table 1.1 Major bioactive compounds in legumes and associated health impacts
Legumes Bioactive compounds Health benefits References
Common bean (P. Tannins, anthocyanins, It can act against the liver injury Ganesan
vulgaris L.) phenolic compounds in animals, breast, colon and and Xu
prostrate cancer (2017)
Lentils Phenolic compounds Benefits against degenerative Ganesan
(Lensculinaris) disorder, type II diabetes, and Xu
coronary heart disease and (2017)
obesity
Soybean Polyphenols such as High antioxidant and antiradical
(Glycinemax (L.) isoflavone, tocopherols, activities, helps in preventing
Merr. Fabaceae) anthocyanin and ascorbic various types of cardiovascular
acid diseases, cancer and osteoporosis
Lima beans Phytochemicals, Radical scavenging activities, Ganesan
(Phaseoluslunatus polyphenols prevent heart disease, and Xu
L.) inflammation, arthritis, and (2017)
immune system decline
Lentils (Lens Phenolic acids, flavanols, Anticancer, angiotensin enzyme Ganesan
culinaris Medik.) flavonols, soy saponins, that reduces the risk of and Xu
phytic acid, condensed cardiovascular diseases, (2017)
tannins coronary heart disease, type II
diabetes, and obesity
Peanut Anthocyanins, Reduces weight gain, Ganesan
(Arachishypogaea proanthrocyanidines and cardiovascular diseases, and Xu
L.) resveratrol Alzheimer’s disease, and cancer (2017)
Peas (Pisumsativum Caffeic, vanillic, Prevent heart disease, anti-­ Ganesan
L.) p-coumaric, ferulic and inflammation, antioxidants and Xu
sinapic acids, quercetin, (2017)
kaempherol, procyanidin
B2 and B3
Adzuki beans Flavanoids, Tocopherols, Inhibit pancreatic Lipase activity Ganesan
(Vigna angularis) and Vitamin E and thus decrease Triglyceride and Xu
concentrations, exert antioxidant (2017)
activity
Mung beans (Vigna Phenolic acid, Source of essential amino acids, Ganesan
radiata L.) Flavanoids, polyphenols Modify Glucose and Lipid and Xu
and Tannins metabolism, exhibits (2017)
hypoglycemic and hypolipidemic
effects, anticancer, anti-­
melanogenesis, hepatoprotective,
and with immunomodulatory
activities

1.3.1 Alkaloids

Alkaloids are group of plant secondary metabolites that protect them against micro-
bial invasions. This class of secondary metabolites comprises of different phytoac-
tive compounds like indo-quinolones, quinolones, agenalsine, indolizidine and
many more. These have potent antimicrobial properties and also act as inhibitors of
8 D. Lahiri et al.

Table 1.2 Major bioactive compounds in legumes and their sources

Antioxidant
Bioactive compounds class Plants Health benefits References
Anthocyanidins, Flavonoids Black bean, Possible Xu et al.
flavonols, flavones, red kidney neuroprotective (2007)
flavan-3-ols, bean, red agents, significant
isoflavonoids, peanut, against Alzheimer’s,
neoflavonoids soybean protection against
cancer, heart disease,
asthma
Caffeic acid, ferulic acid, Phenolic acids Bean, black Prevent cellular Xu et al.
procatechuic, gallic bean, damage, promote (2007)
acids, syringic acids, cowpea, anti-inflammatory
p-hydroxybenzoic, lentil, lima conditions, protection
p-coumaric, sinapic bean, red against free radicals
acids, vanillic acid kidney
Condensed tannins, Tannins Chick pea, Improved immune Scalbert
hydrolysable tannins green pea, response, and blood et al.
common sugar balance (2005)
bean,
yellow pea,
lentil,
soybean
Phytic acids or Phytate Phytic acid Most of the Prevent the formation Barahuie
Vigna spp. of cavities, plaque and et al.
tartar in the teeth, has (2017)
hypoglycemic effects,
reduce the formation
of kidney stones.
GABA γ-Aminobutyric Adzuki Effective for the Ganesan
acid (GABA) beans, treatment of and Xu
mung beans sleeplessness, (2017)
depression, autonomic
disorders

biofilms. Alkaloid like 1,3,4-oxadiazole helps in inhibiting the quorum sensing pre-
cursor molecule like 2-heptyl-4-quinolone (HHQ), the virulence effect of some
organisms and the gene responsible for swarming motility can be inhibited in the
presence of 7-hydroxyindole. Many alkaloids within the legumes act as neuromodu-
lators and possess neurotoxic activities to repel the herbivorous animals. Alkaloid
like squalamine has a potent antibacterial effect and it kills the bacterial cells by
destroying the cell membranes. The squalamine binds to the receptor present on the
exposed cell surface by penetrating through the lipopolysaccharide layer of the cell
membrane resulting in the inhibition of cell membrane synthesis (Salmi et al. 2008).
Electrostatic force of attraction helps in holding the squalamine with the receptors
present on the bacterial cell surface. The cell membrane comprises of large quanti-
ties of free negatively charged ions that induce strong interactions with the drug like
compounds (Cushnie et al. 2014). Alkaloids like isoquinolone, obtained from
1 An Introduction to Legume Biotechnology 9

legume plant species like Thalictrum minus acts as a ligand for DNA and has the
ability to get attached both with double stranded and single stranded DNA mole-
cule. It has the ability to break down the highly conserved bacterial proteins Ftsz.
Ftsz-GFPase results in the formation of Z-ring (Boberek et al. 2010). Another mode
of action of these alkaloids like isoquinoline is to inhibit the synthesis of nucleic
acid by inhibiting the activities of topoisomerase I and II, and on the other hand
substituted quinolines like methyl quinolones prevents the bacterial cell prolifera-
tion by hindering oxygen uptake by the cells (Tominaga et al. 2002).

1.3.2 Terpenoids

These are the group of secondary metabolites that contains a 5-C isoprene units.
Most of the active compounds present in this group comprises of cyclic structure
that differs from one another in possessing functional groups within their ring
(Harborne 1973). Classification of terpenoids is generally based on the number of
isoprene units present into hemi-terpenoids, monoterpenoids, sesquiterpenoids,
diterpenoids, triterpenoids, tetra terpenoids and carotenoids. Their therapeutic prop-
erties like anti-bacterial, anti-fungal, anti-viral, anti-protozoan, anti-allergens and
anticancer effects are quite pronounced and are strongly reported (Mackeen et al.
1997). Presence of terpenoids is reported from many living organisms throughout
nature, especially in plants where it is considered to be the major content of the
natural products, in marine animals and fungi. Terpenoids support the basic func-
tions of plants including growth, development and wound repair. In medicinal
plants, different types of terpenoids are found like oleanolic acid, ursolic acid, car-
vacrol etc. Terpenoids are also of commercial importance due to their use in food
and cosmetics industries as flavouring agents and fragrances. Ursolic acid, a sec-
ondary metabolite that is generally present in leaves, stem bark and fruit peels is a
pentacyclic terpenoid (isomer of oleanolic acid) which has a wide range of pharma-
ceutical implications. Ursolic acid has pharmacological activities like anti-fertility
effects, antibacterial activity against Pneumococci, Staphylococci and Streptococcus
mutans, and antihelmintic activity (Ali et al. 1996). Oleanolic acid is a pentacyclic
triterpenoid and its derivatives possess several therapeutic effects like antioxidant,
anticancer, anti-inflammatory and hepatoprotective effects. Oleanolic acid safe-
guards the plants by formation of barrier against water loss and pathogens. Also,
other therapeutic properties of oleanolic acid include antiviral activity, antibacterial
property against S. aureus, S. mutans, B. subtilis, M. tuberculosis, P. aeruginosa
etc., and antiprotozoal activity (Abdullah et al. 2013). Carvacrol, an essential aro-
matic compound found in plants like thyme, oregano, pepperwort, wild bergamot is
a phenolic monoterpenoid that is capable of offering pleasant smell and taste. Some
of their uses also include antibacterial and antifungal activity. Moreover it is reported
in treating fever, pneumonia, nail fungus, cholecystitis and cholangitis (Abdullah
et al. 2013).
10 D. Lahiri et al.

1.3.3 Coumarins

Coumarins, isolated from Tonka beans, are a group of colourless and crystalline
phytochemical, polyphenolic compounds. They are either free or glucose combined
oxygen heterocycles. Their pharmacological, biochemical and therapeutic applica-
tions are mainly due to the substitution pattern of their pyrone classes. Coumarins
are widely divided into four clusters namely simple coumarins, pyrone substituted
coumarins, pyranocoumarins, and furanocoumarins. These coumarins are found
abundantly in fruits, roots, stems, leaves and also in Umbelliferone and in Rutaceae
family. Their presence is also traced in selective microorganisms like Streptomycin,
aflatoxin from Aspergillus sp. etc. Their importance in the use as medicine for treat-
ment of various clinical conditions alongside significant effect on physiological,
anti-tumor and bacteriostatic activity has been reported. Furthermore, their potential
therapeutic applications in treating chronic infections, oedema and anticoagulant,
anticancer, anti-inflammation, analgesic, antidiabetic, anti-neurodegenerative activ-
ities are also significant. Esculetin, another simple coumarins has antitussive
aspects. Furthermore, it’s antibacterial, anti-tumor, anti-­inflammatory, antioxidative
and neuroprotective properties has made Esculetin as one of the most promising
leads for various chemists to develop variety of drugs (Yaacob 1987).

1.3.4 Polyphenols

These are secondary metabolites widely distributed in various plant parts of cereals
and beverages that are involved in defence against pathogenic aggregation or UV
radiation (Yaacob 1987). The main classes of polyphenols which are conjugated
forms with one or more sugar residues linked to hydroxyl groups, include phenolic
acids, lignans, flavonoids and stilbenes. They are the key contributors in the color,
odor, bitterness, and oxidative stability in food. Phenylalanine, a common interme-
diate in more than 8000 identified polyphenolic compounds, have therapeutic uses
due to their properties like antidiabetic, anti-aging, cardioprotective, treatment from
infections, asthma, hyper-tension, anticancer and other properties. They mainly
consist of p-coumaric, caffeic acid, ferulic acid, and sinapic acids. Studies show that
in polyphenol rich foods, polyphenolic compounds are responsible for treatment of
chronic human diseases, increase antioxidant capacity and are known to have thera-
peutic vitality (Yaacob 1987).
General subclass of polyphenols includes: flavanols, flavanones, flavones, isofla-
vones and anthocyanins. Polyphenols include bioactive compounds like curcumin,
rosmarinic acid, gingerol, shagaol etc. Curcumin (diferuloylmethane) is a polyphe-
nol compound isolated from ground rhizomes of the plant (Curcuma longa) L. that
has been extensively used in ayurvedic medicine over centuries as a nontoxic agent,
with a variety of therapeutic properties like analgesic, anti-inflammatory, antioxi-
dant, antiseptic, antifungal, antibacterial and antiplatelet activity (Qader et al. 2012).
1 An Introduction to Legume Biotechnology 11

Rosmarinic acid is an ester of caffeic acid that occurs mostly in perilla, sweet basil
and rosemary (Yaacob 1987). Understanding the contribution towards human health
and nutrition, shogaols and gingerols stands out as the major pungent compounds
present in ginger (Zingiber officinale) (Baharum et al. 2010). Shogaols act as impor-
tant biomarkers for the quality control of numerous ginger-containing products, due
to their effectiveness in the treatment of inflammation, anticancer, dyspepsia, nau-
sea, vomiting, etc. (Costerton 2007).

1.3.5 Sulphur-Containing Bioactive Compounds

The legumes are comprised of sulphur containing active compounds showing potent
antibacterial properties like isothiocyanates, ajoene and allicin. They have proved
their effectiveness against a wide range of microbial species like Enterococcus fae-
calis, S. mutans, Prevotella nigrescens, Aggregatibacter actinomycetemcomitans
and Clostridium perfringens. It has been observed that the effectiveness of these
bioactive compounds vary greatly from the source where they have been isolated.
Isothiocyanates have even shown its effectiveness against Methicillin resistant
Staphylococcus aureus species (Dias et al. 2012). Research has shown that allicin
synergistically reacts with omeprazole to bring about its impact upon the target
microbial species. Thus the synergistic effects of these bioactive compounds are
showing a better path of replacing antibiotics.

1.3.6 Bioactive Compounds of Edible Legumes

Isoflavones stand out to be the most important and vividly studied bioactive com-
pound of legumes, which together with procyanidins and phenolic acids constitute
the vital phenolic compounds present in seeds. Estradiol-17 beta molecules are the
group of isoflavones that has equivalent effect as that of oestrogen which has similar
affectivity as that of commercially available drug molecules (Sorensen et al. 2005).
They can also act effectively against various cancerous cells specially the endothe-
lial and breast cancer (Agbafor and Nwachukwu 2011). Soy food (legume product)
lowers the risk of prostate and colorectal cancer. Relatively higher content of antho-
cyanin and proanthocyanidins or condensed tannins are present as phenolic com-
pounds with antioxidant potential in dark coloured seeds rather than those of pale
coloured seeds. Legume seeds also contain different carotenoids, being lutein, the
predominant one in economically important grain legumes, such as chickpea, lentil,
soybean, peanut, cowpea, pea, faba bean, and lupin, followed by zeaxanthin and
β-carotene. γ-Tocopherol is found as the most abundant isoform in lentils, soybean,,
broad bean, and some lupin species (Wan Hassan 2006; Bunawan et al. 2011; Almey
et al. 2010; Uyub et al. 2010) (Table 1.3).
12 D. Lahiri et al.

Table 1.3 Major Secondary metabolites from legumes and their mechanisms of action
Secondary Origin of Examples from Refer
metabolites occurrence Activity Fabaceae ences
β-Carboline Petalostyles Serotonin receptor Harman, harmalan, Ganesan
alkaloids labicheoides, agonist DNA tetrahydroharman, and Xu
Acacia complanata, intercalation; leptocladine (2017)
Burkea africana, mutagenic
Prosopis nigra,
Desmodium
gangeticum
Indolizidine Astragaleae; Inhibits endoplasmic Swainsonine, Ganesan
alkaloids Castanospermum hydrolases castanospermine and Xu
(2017)
Piperidine Genistoid clade Causes malformations Ammodendrine Ganesan
alkaloids in embryos and Xu
(2017)
Pyridine In all subfamilies; Antimicrobial, Trigonelline Ganesan
alkaloids abundant in IRLC bactericidal and Xu
clade and (2017)
Phaseoleaesens. lat.
Pyrrolizidine Crotalaria; Mutagenic and Monocrotaline, Ganesan
alkaloids (PA) Lotononis carcinogenic as they senecionine and Xu
modulate several (2017)
neuroreceptors, like
5HT2, mACh, GABA,
D2 and α2.
Quinolizidine Genistoid clade; Modulate nAChR and Sparteine, lupanine, Ganesan
alkaloids Ormosia clade; mAChR; Na + channel anagyrine, cytisine, and Xu
(QA) Sophora blocker, neurotoxic in matrine, lupinine (2017)
secundiflora; Calia, nature
Bolusanthus
Antimicrobial Adenanthera spp. Potent antimicrobial ApDef1 Ganesan
peptides and Xu
(AMP) (2017)
Amylase Delonix regia, Control the Antidiabatic Ganesan
inhibitor Vigna sp. postprandial increase of and Xu
blood glucose (2017)
Protease Several Fabaceae Inhibits trypsin mainly Trypsin inhibitors Ganesan
inhibitors in herbivores and Anticarcinogenic and Xu
(2017)
Oligo Vigna sp. Reduce colon cancer Prebiotic Ganesan
saccharide by reducing and Xu
composition of mucin (2017)
in colonic cancer
Lectins Abrus precatorius, Inhibitors of ribosomal Abrin, robin Ganesan
Robinia protein biosynthesis and Xu
(2017)
(continued)
1 An Introduction to Legume Biotechnology 13

Table 1.3 (continued)

Secondary Origin of Examples from Refer
metabolites occurrence Activity Fabaceae ences
Tannins Mostly trees Antimicrobial and Mostly catechin type Ganesan
anti-herbivore activities and Xu
(2017)
Phytate Vigna sp. Hypocholesterolaemic Inositol Ganesan
effect, antic hexaphosphate, or and Xu
arcinogenic and also IP6 (2017)
protect
DNA damage
Phenyl Mainly Acacia spp.; Psychoactive N-Methyl Ganesan
ethylamines Caesalpininoideae phenylethylamine; and Xu
(2017)
Polyamines Mainly Phaseoleae Growth regulator Spermine, spermidine Ganesan
and Xu
(2017)
Tryptamines Mimosoideae Agonist towards N,N-­ Ganesan
Serotonin receptor; Dimethyltryptamine; and Xu
hallucinogenic bufotenin; (2017)
N-methyltryptamine
Tyramines Mimosoideae, Psychoactive; inhibit N-Methyltyramine; Ganesan
Desmodieae insect feeding hordenine; and Xu
N-methylmescaline (2017)
Simple Widely distributed Antioxidants; Vanillin, syringic Ganesan
phenols antimicrobial acid, ferulic acid, and Xu
gentisic acid, gallic (2017)
acid, p-hydroxy
benzaldehyde
Flavonoids Widely distributed, Antimicrobial and Quercetin, Ganesan
in all tribes anti-herbivore kaempferol, etc. and Xu
activities; antioxidants (2017)
Protein Vigna sp. Anti-HIV activity, help Angularin, delandin Ganesan
against fungal and unguilin and Xu
pathogenesis (2017)

1.4 Availability of Trace Elements Within the Legumes

Legumes contain a large amount of trace elements like copper, iron, zinc and manga-
nese. These trace elements not only maintain the health of the consumers but also
provide nutritional supplements to the body. These trace elements also act as immune
boosters and help in the maintenance of gastrointestinal mucosal integrity. The pre-
dominant element found within the leguminous seeds is iron. The amino acids like
cysteine, fructose and citric acids help in increasing greater uptake of iron from the
soil whereas compounds like phytate, oxalate and polyphenols act as inhibitors to the
absorption of calcium from soil (Sandberg 2002). Commonly available amino acids
like cysteine and histidine are promoters for the absorption of zinc from the soil
whereas phytate, ethylenediaminetetraacetic acid, oxalate and fibres inhibit the bio-
availability of zinc from the soil.
14 D. Lahiri et al.

1.5  ffect of Biotic Stress on the Yield of Bioactive

E
Compounds of Legumes

Symbiotic relations between the soil-born bacteria (rhizobia) and leguminous plants
helps enhance the quality and productivity of agricultural crops thereby enhancing the
animal/human nutrition and health (Graham and Vance 2003). While staying in the
roots of the plant, these bacteria helps the plants in nitrogen fixation and protects
against various microbial pathogens (Chakraborty et al. 2003). These symbiotic inter-
actions have strongly driven the investigation towards a number of biotic (bacteria,
fungi, viruses, insects, nematodes) stress factors thereby affecting the yield of agricul-
tural crops.

1.5.1  ole of Microorganisms in Increasing the Bioactive

R
Compound Content of Legumes
1.5.1.1 Arbuscular Mycorrhizae Fungi (AMF)

Arbuscular mycorrhizal fungi (AMF) shares symbiotic relation with plants and are
responsible for activating different biosynthetic pathways like shikimic and malonic
pathways as explained by Gor et al. (2011). Alteration in these pathways lead to
alteration of the production of phenolic, terpenes and alkaloids in plants thereby
affecting directly or indirectly the quality of food, medicinal plants or spices
(Bunawan et al. 2011; Almey et al. 2010). For example, a significant increase in
β-caryophyllene and pinene in coriander was observed by Kapoor et al. (2002)
when inoculated with G. macrocarpum. Secondary metabolites such as allicin, was
found to increase in garlic plants when inoculated with G. fasciculatum. Cultivars
inoculated with AMF such as basil and Purple petra were found to have elevated
concentration of anthocyanins. A significant rise in concentrations of carotenoids
and total phenolic compounds were observed in tomato inoculated with AMF
(Glomus sp.). In addition to fungi like AMF, soil microbiome can also act synergis-
tically to increase some secondary metabolites. In one study, it was observed that
the use of fungal consortium causes significant rise in carotenes and xanthophylls of
Capsicum annuum L (Mena-Violante et al. 2006). In addition to the production of
secondary metabolites as defence mechanism, plants also produces enzymes related
to metabolic pathways. For example, inoculating M. truncatula and M. sativa roots
with AMF (Glomus versiforme) resulted in rise in concentration of chalcone syn-
thase (CHS), phenylalanine ammonia lyase (PAL) and isoflavone reductase (IFR)
transcript levels. In another study, inoculation of barley roots with AMF resulted in
increased production of endogenous jasmonic acid (Hause et al. 2002).
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