ANALYSIS OF DROUGHT AND RUST DISEASES TOLERANCE CONFERRED BY ENDOPHYTES IN WHEAT CROP By HAFIZ ARSLAN ANWAAR M.Sc. (Hons.) Plant Pathology 2005-ag-1757 A thesis submitted in partial fulfilment of the requirements for the degree of DOCTOR OF PHILOSOPHY IN PLANT PATHOLOGY Department of Plant Pathology Faculty of Agriculture i
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ANALYSIS OF DROUGHT AND RUST DISEASES TOLERANCE CONFERRED BY ENDOPHYTES IN
WHEAT CROP
By
HAFIZ ARSLAN ANWAAR
M.Sc. (Hons.) Plant Pathology2005-ag-1757
A thesis submitted in partial fulfilment of the requirements for the degree
of
DOCTOR OF PHILOSOPHY
INPLANT PATHOLOGY
Department of Plant PathologyFaculty of Agriculture
University of Agriculture, Faisalabad
2018
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DEDICATED TO
Our national political leader
IMRAN KHAN
A SYNONYMOUS OF CHANGE
MAN OF COMMITMENT, STRUGGLING AGAINST CORRUPT VULTURES.
A LONG AWAITED RAY OF HOPE FOR PITIABLE PAKISTANI NATION GRANTED AFTER GREAT QUID M.A JINNAH.
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ACKNOWLEDGEMENTSAll the praises and thanks for ALMIGHTY ALLAH, who bestowed me with the
opportunity and ability to contribute a little material to the existing knowledge. Trembling
lips and wets eyes praises for Holy prophet, MUHAMMAD (PBUH) who is the thriving
city of knowledge.
Words don’t come easy for me to articulate the feelings of unassuming admiration
to the great scholar of this era SYED ABU ALA MODOODI (R.H). He behaved a torch
of guidance and knowledge for me and impart that “Islam a complete code of life” is not
a utopia and get rid from sectarianism.
I would like to thanks to my supervisors Dr. Safdar Ali and Prof. Dr. Shahbaz
Talib Sahi for their valuable comments, guidance and continuous support during my
Ph.D. studies and research work. I also express my deep gratitude to Dr. Ye Xia, Ohio
State University, Columbus, USA for sharing valuable ideas. No acknowledgement
could ever express my obligation to my affectionate PARENTS whose endless efforts
and encouragements sustained me all stages of my life and whose hands always rose in
prayers for my success.
I shall be missing something if I don’t extend my admiration and appreciation to
my fellows and friends Dr Sahibzada Rizwan and Dr Hafiz Sajid for their support, lot
of smiles and enjoyable moments throughout my Ph.D. study period. Special thanks to
Zubair Safdar for making some arrangement of financial assistance as well as my
colleague Dr Safdar Hussain for assistance in writing of this manuscript.
Hafiz Arslan Anwaar
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List of contentsCHAPTER TITLE PAGE
1 INTRODUCTION 12 REVIEW OF LITERATURE 5
2.1 Origin and geographical significance of wheat 52.2 Economic importance and taxonomic status of the wheat 52.3 Significance of wheat in Pakistan 62.4 Wheat productivity constraints 62.5 Impact of drought on wheat genotypes 72.6 Effects of terminal drought 7
2.6.1 Leaf Senescence 72.6.2 Light harvesting and fixation of carbon 72.6.3 Grain development 82.7 Tolerance to terminal drought 8
2.7.1 Drought escape 92.7.2 Solute accumulation and osmotic adjustment 92.7.3 Antioxidant defence 92.7.4 Stay green 102.7.5 Root system architecture 102.7.6 Reserve translocation 102.7.7 Hormonal regulations 112.8 Role of rusts in wheat yield reduction 112.9 Historic epidemics and yield losses 122.10 Classification and life Cycle of Puccinia 132.11 Symbiosis 142.12 Plant Symbionts 152.13 Endophytism 152.14 Endophytism VS Pathogenism 162.15 Classification of endophytes 172.16 Fungal endophytes 172.17 Fungal endophytes diversity 17
2.17.1 Class 1 endophytes 182.17.2 Class 2 endophytes 182.17.3 Class 3 endophytes 192.17.4 Class 4 endophytes 19
2.18Mechanisms of endophytic fungi confer tolerance against abiotic stresses 19
2.19Mechanisms of endophytic fungi confer tolerance against biotic stresses 20
2.20Role of fungal endophytes in conferring plant tolerance against different abiotic and biotic stresses 21
2.20.3 Colletotrichum 263 MATERIALS AND METHODS 28
3.1 Experimental site and conditions 283.2 Collection of wheat germplasm 283.3 Screening of wheat germplasm against drought 293.4 Screening of wheat germplasm against rust diseases 303.5 Rust inoculation Procedures 30
3.5.1 Collection of inoculums 303.5.2 Storage of inoculums 313.5.3 Methods of inoculation 31
3.6 Data recording of leaf and stripe rust 333.7 Rusts screening of wheat genotypes 333.8 Yield and yield components 34
3.8.1 Number of tillers m-2 343.8.2 Number of productive tillers 343.8.3 Number of grains per spike 343.8.4 Thousand grains weight (g) 348.8.5 Biological yield (gm-2) 343.8.6 Grains yield (gm-2) 343.8.7 Harvest index (%) 358.8.8 Percent yield reduction (%) 353.8.9 Percent yield increased (%) 353.8.10 Area under disease progress curve (AUDPC) 353.8.11 Coefficient of infection (CI) 35
3.9Optimization of efficient and compatible endophytes with wheat seed 35
3.9.1 Collection of samples for endophytes 353.9.2 Morphological identification and mass culturing of endophytes 363.9.3 In-vitro evaluation of endophytes 36
3.10Field appraisal of selected efficient and compatible endophytes against drought and rust diseases 36
3.11 Statistical analysis 374 RESULTS AND DISCUSSIONS 38
4.1 Response of different wheat genotypes against drought stress. 384.1.1 Number of grains per spike 384.1.2 1000-grains weight (g) 394.1.3 Number of productive tillers 394.1.4 Harvest index (%) 504.1.5 Biological yield (gm-2) 504.1.6 Grain yield (gm-2) 524.1.7 Drought sensitivity indices 54
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4.2 Response of different wheat genotypes against Leaf rust 574.2.1 Disease severity (%) 574.2.2 Area under disease progress curve (AUDPC) 594.2.3 Coefficient of infection (CI) 614.3 Response of different wheat genotypes against yellow rust 63
4.3.1 Disease severity (%) 634.3.2 Area under disease progress curve (AUDPC) 664.3.3 Coefficient of infection (CI) 68
4.4Symbiotic effect of fungal endophytes on two drought sensitive wheat genotypes in drought conditions 70
List of TablesTable 3.1 Wheat genotypes used in the screening experiment 29Table 4.1 Influences of drought stress on the yield related traits of different
wheat genotypesTable 4.2 Analysis of variance for morphological traits of wheat in normal
and drought stress conditions43
Table 4.3 Influence of drought stress on the yield related traits of biological yield (gm-2) and Harvest Index %
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Table 4.4 Influences of drought stress on the yield related traits of GY, YR%, TOL, MP and SSI
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Table 4.5 Impacts of wheat leaf rust on FDS, AUDPC and CI in field conditions
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Table 4.6 Analysis of variance for FDS, AUDPC and CI under field conditions
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Table 4.7 Impacts of yellow rust on traits of FDS, AUDPC and CI in field conditions
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Table 4.8 Analysis of variance for FDS, AUDPC and CI under field conditions
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Table 4.9 Symbiotic effects of endophytes for 1000-grain weight in tolerance of drought stress
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Table 4.10 Symbiotic effects of endophytes for Number of Productive Tillers in tolerance of drought stress
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Table 4.11 Symbiotic effects of endophytes for biological yield in tolerance of drought stress
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Table 4.12 Symbiotic effects of endophytes for grain yield in tolerance of drought stress
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Table 4.13 Analysis of variance for TGW, PT, BY, GY and YI% under field conditions
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Table 4.14 Symbiotic effects of endophytes for percent yield increased in tolerance of drought stress
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Table 4.15 Antagonistic effects of endophytes for disease severity in tolerance of disease (leaf rust) conditions
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Table 4.16 Antagonistic effects of endophytes for AUDPC in tolerance of disease (leaf rust) conditions
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Table 4.17 Analysis of variance for FDS, AUDPC, TGW, GY and YI% under field conditions
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Table 4.18 Symbiotic effects of endophytes for 1000-grain weight in tolerance of disease (leaf rust) conditions
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Table 4.19 Symbiotic effects of endophytes for grain yield in tolerance of disease (leaf rust) conditions
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Table 4.20 Symbiotic effects of endophytes for percent grain yield increase in tolerance of disease (leaf rust) conditions
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Table 4.21 Antagonistic effects of endophytes for disease severity in tolerance of disease (yellow rust) conditions
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Table 4.22 Antagonistic effects of endophytes for AUDPC in tolerance of disease (yellow rust) conditions
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Table 4.23 Analysis of variance for FDS, AUDPC, TGW, GY and YI% 84
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under field conditionsTable 4.24 Symbiotic effects of endophytes for 1000-grain weight in
tolerance of disease (yellow rust) conditions85
Table 4.25 Symbiotic effects of endophytes for grain yield in tolerance of disease (yellow rust) conditions
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Table 4.26 Symbiotic effects of endophytes for percent grain yield increase in tolerance of disease (yellow rust) conditions
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List of FiguresFig 2.1 Life cycle of Rust 13Fig 2.2 Life cycle of Puccinia 14
Fig 3.1 Modified diagrammatic Cobb Scale described by Peterson et al., 1948 31Fig 3.2 Artificial inoculums of leaf rust (left) and yellow rust (right) 32Fig 3.3 Field view of Leaf rust (left) and Yellow rust (right) 34Fig 4.1 Comparison of 50 wheat genotypes for No. of grains per spike
under normal and drought conditions44
Fig 4.2 Comparison of 50 wheat genotypes for No. of productive tillers under normal and drought conditions
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Fig 4.3 Comparison of 50 wheat genotypes for 1000-grains weight under normal and drought conditions
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Fig 4.4 Comparison of 50 wheat genotypes for Biological yield (gm-2) under normal and drought conditions
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Fig 4.5 Comparison of 50 wheat genotypes for Grain yield (gm-2) under normal and drought conditions
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Fig 4.6 Comparison of 50 wheat genotypes for Harvest index (%) under normal and drought conditions
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LIST OF ABBREVIATIONS
ABBREVIATIONS Meanings
AARI Ayub Agricultural Research Institute
ABA Abscisic Acid
AMF Arbuscular mycorrhiza fungi
ANOVA Analysis of Variance
APX Ascorbate peroxidase
AUDPC Area under disease progress curve
BY Biological yield
CAT Catalase
CEs Clavicipitaceous endophytes
CI Coefficient of Infection
CIMMYT International maize and Wheat improvement centre
CRD Completely Randomized Design
DON Deoxynivalenol
DSE Darkly melanized septa
FAO Food and Agriculture Organization
FDS Final Disease Severity
FHB Fusarium head blight
GY Grain yield
HI Harvest Index
IAA Indole acetic acid
ISR Induced systemic resistance
LSD Least Significant Difference
MHB Mycorrhization helper bacteria
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MP Mean Productivity
NCEs Non-clavicepataceous endophytes
NUE Nitrogen used efficiency
P. indica Piriformospora indica
PGPB Plant growth promoting bacteria
PGPR Plant growth promoting rhizobacteria
POX Peroxidase
PT Productive Tillers
RCBD Randomized complete block design
ROS Reactive Oxygen Specie
RuBP Ribulose bisphosphate
SOD Superoxide dismutase
SSI Stress Susceptibility Index
TGW Thousand grain weight
TOL Tolerance Index
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ABSTRACT
Excessive use of pesticides has caused agricultural and environmental hazards. Microbial inoculation is an alternate to pesticides for confronting pathogens and is an environmental friendly approach. Endophytes are beneficial microbes and biologically safe for inducing tolerance in plants. Hence, the current research was conducted to evaluate endophytes potential in wheat against drought stress and rust diseases. Fifty genotypes of wheat were sown under Randomized Complete Block Design (RCBD) in field conditions for evaluation against rust diseases and drought conditions. The drought stress was given to the wheat genotypes by skipping the irrigation at flowering and grain filling stage for drought resistance whereas all genotypes were also inoculated against rust diseases through natural and artificial method at tillering and heading stage. Data regarding drought stress were recorded on the basis of different growth parameters viz. number of grains per spike, 1000-grain weight (g), number of productive tillers m2, biological yield (gm-2), grain yield (gm-2), harvest index % and percent yield reduction, drought tolerance indices like mean productivity (MP), tolerance index (TOL) and stress susceptibility index (SSI). Data regarding final disease severity percentage, area under disease progress curve and coefficient of infection were recorded for rust diseases. Kohsar-95 and Parwaz-94 exhibited most drought sensitive genotypes while two leaf rust (Faisalabad-85, Aas-02) and two yellow rust genotypes viz. Fareed-06 and Shafaq-06 expressed susceptible response. Plant samples for endophytes were collected from desert areas (Cholistan, Thar and Rohi) of Pakistan. The endophytes were isolated, identified and purified in Plant Mycology Lab. on sterilized Potato Dextrose Agar media (PDA). The in-vitro efficacy of endophytes was evaluated in test tubes containing 0.3% agar concentration. The wheat seed was sown in test tube containing distilled water along with fungal spore suspensions (1×106/ml) and incubated at 28±2oC. The root and shoot length was measured after 4 days of interval. The four endophytes expressed significant results were used for further studies. Spore suspensions of these endophytes were prepared and their concentrations were observed through haemocytometer. Seeds of disease and drought susceptible wheat genotypes were inoculated by dipping in spore suspension and sown in field under factorial RCBD. Inoculated susceptible wheat genotypes exhibited the tolerance against drought and rust diseases. The endophyte Piriformospora indica showed significant increase in grain yield 15.4% of drought sensitive genotypes followed by Colletotrichum lindemuthianum, Trichoderma viride, and Acremonium lolii 11.3 %, 8.1 % and 7.5 % respectively. Similarly, for leaf and yellow rust diseases P. indica also exhibited statistically significant increase in grain yield 17.5% and 12.3%, respectively followed by Trichoderma spp. (13.7 % and 10.6 %). Colletotrichum spp. and Acremonium spp. showed (7.1%, 6.2%) as well as (8.2%, 4.2%) under leaf rust and yellow rust conditions respectively.
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CHAPTER 1 INTRODUCTION
Pakistan is an agricultural country. A huge section of the population is dependent
directly or indirectly on agriculture. The trade of Pakistan totally depends on agriculture.
The food security is highly focused on obtaining more food to fulfil the needs of
burgeoning population which can only be accomplished when the production of cereal
crops is increased globally. Wheat (Triticum aestivum L.) belongs to family Poaceae and
is extensively cultivated in the majority of the world regions. In Pakistan, wheat as main
staple food, is cultivated on the area of 9.23 million hectare with the estimated production
of 25.3 million metric tons with 2.74 metric tons/ha grain yield (USDA, 2017; Pakistan
Bureau of Statistics, 2017)
The yield of cereal crops is very low in Pakistan as compared to developed
countries due to many abiotic and biotic constraints. Biotic (diseases and insect pest) and
abiotic stresses (drought, temperature, salinity and water logging) for crop are highly
concerned in this regard (Hussain et al., 2015). Faced with scarcity of water resources,
only a single factor of drought is utmost uncertain hazard to food security of world. It has
been the catalyst of the past’s worse famines (Loewenberg, 2014). The drought severity
is unpredictable as it is influenced by rainfall, evaporation and soils’ moisture storing
capacity (Muscolo et al., 2015; Ramirez et al., 2015).
The drought incidence and severity will certainly increase in coming future as a
result of global warming that will direct towards a rigorous decline in overall production
of food. Predicted temperature rise of 1.5-5.8 °C by 2100 will lead ruthless troubles for
agricultural production (IPCC, 2012). At the same time progressively increasing human
population that might achieve to nine billion in 2050, requires a surge in food supplies.
Since desertification swells further by reason of constant trouncing of arable area the
condition will be shattering and distressing more in the upcoming days (IPCC, 2007;
2012).
Drought conditions impact an influential demerit of low wheat productivity.
Drought reduces the number of fertile tillers which are main contributors of grain yield
(Al- Ajlouni et al., 2016). Drought deters cell enlargement and cell division and also
reduces respiration, photosynthesis, translocation, nutrient metabolism, ion uptake and
carbohydrates (Farooq et al., 2008). Severe water stress upsets plant water relations and
reduces water-use efficiency which ultimately causes decline of photosynthesis decline,
metabolism disorder and thus results in plant death (Jaleel et al., 2009; Cattivelli et al.,
1
2008; Sikuku et al., 2012). All the wheat growth phonological stages may affected by
drought and the stages of reproductive and grain-filling are the most responsive (Pradhan
et al., 2012; Nawaz et al., 2013).
Terminal drought causes significant yield reductions in wheat because of
oxidative damage to photo-assimilatory machinery (Farooq et al., 2009), accelerated leaf
senescence (Yang et al., 2007), pollen sterility (Dorion et al., 1996; Cattivelli et al.,
2008), decreased rates of fixation of carbon and translocation of assimilates (Asada,
2006), decreased set of grains and their development (Ahmadi and Baker, 2001; Nawaz
et al., 2013) and condensed sink capacity (Liang et al., 2001). Drought at post-anthesis
lessen the wheat yields by 1-30%, mild stress at heading stage losses 57%, whereas
persistent terminal drought shrinks the grain yields by 58–92% (Dias de Oliveria et al.,
2013).
Massive losses in wheat yield are attributed to various diseases in which rusts
have caused huge yield losses in the recent years. New races of rusts are evolving
unremittingly day by day which have infected the resistant varieties (Brian, 2006). Leaf
or brown rust, stem or black rust and yellow or stripe rusts are generally observed in
wheat. Leaf rust of wheat caused by the fungus Puccinia recondita infects the leaf blades,
leaf sheaths and glumes in vulnerable genotypes (Huerta-Espino et al., 2011). As a result
decline the number of grains per spike and grain weight (Kolmer et al., 2005; Marasas et
al., 2004). Early infection of leaf rust in wheat usually reasons high yield losses; infection
of 60–70% on the flag leaf at emergence of spike may cause more than 30% yield losses.
Stem or black rust caused by Puccinia graminis is the most destructive disease of wheat.
In the presence of favourable conditions, it causes up to 100 % yield losses in susceptible
wheat genotypes (Roelfs, 1985; Leonard and Szabo, 2005). Stripe rust caused by
Puccinia striformis is the most significant favoured mild winter, cool summer and long
cool and wet spring. The yield losses of 10-70% on wheat depend on susceptibility of the
genotypes, initial infections, inoculum density and inoculum multiplication rate (Chen,
2005).
Plants combat different abiotic stresses by their own natural defence and in
cooperation with different soil microorganisms (Marulanda et al., 2006). Activities of
microorganisms facilitate in continuance of biological equilibrium and soil’s
sustainability in stresses (Sieber et al., 2005; Alexander, 2005; Kavamura et al., 2013).
Endophytes are fungal or bacterial microbes that colonize healthy plant tissue
intracellularly and intercellularly without causing any obvious disease symptoms
2
(Bandara et al., 2006; Castillo et al., 2006; Azevedo et al., 2000). They are ubiquitous,
colonize the plants which are isolated from almost all species of plants examined to date
(Mohali et al., 2005; Zhang et al., 2006). Their symbiotic and mutualistic association can
be obligate or facultative and causes no harm to the host plants. Endophytic
microorganisms induce defence mechanisms in host plants to counteract pathogen attack
and others generated antibiotic substances that hamper growth of pathogen, competition
for host resources and space may also take place between incoming pathogens and
already existent endophytes (Arnold et al., 2007; Wang et al., 2007).
Endophytes are also playing their imperative role for mutual interaction with their
hosts for better adaptability and systemic resistance, augmenting nutrient uptake, stress
tolerance, balancing minerals concentration and composition, bolstering abiotic and
pathogenic tolerance or resistance (Redman et al., 2011; Kavamura et al., 2013). The
constructive and valuable characteristics of endophytic fungi have observed in host plants
against numerous stresses (Waller et al., 2005; Rodriguez et al., 2008; Hamilton et al.,
2010). The endophytes also play a considerable function in food safety, bioremediation
and sustainable crop production (Ganely et al., 2006; Singh et al., 2011).
So, to enhance farmers' earnings and productivity of wheat, appropriate strategies
might be adopted to minimize severe yield losses by different abiotic stresses and
pathogenic diseases. Numerous scientists and researchers are discovering sustainable
alternative approaches to pesticides and chemical fertilizers. Natural resources are
decreasing with the passage of time due to spontaneously increasing world population. It
is need of the hour to find out an alternative approach for growing more food in such a
manner that can reduce detrimental environmental impacts of intensive farming,
fungicide resistance and environmental pollution.
The beneficial effects of endophytes on plants against diseases have increased the
interest of researchers and farmers for enhancing agricultural production. This bio-control
strategy for combating different a biotic stresses and pathogenic diseases have altered the
attention of farmers for better crop production. It is tried to discover different efficient
and compatible fungal endophytes for wheat tolerance against drought and rust diseases.
The present research was conducted to achieve the following objectives:
To screen out resistant and sensitive / susceptible genotypes of wheat against
drought and rust diseases
3
To find out efficient and compatible endophytes for wheat tolerance against
drought and rust diseases
To meet the above stated objectives the following line of work was adopted
a) Seed collection of different wheat genotypes
b) Screening of resistant and sensitive / susceptible genotype of wheat against
drought and rust diseases
c) Collection and isolation of fungal endophytes
d) In-vitro evaluation of efficient and compatible endophytes for wheat
e) Preparation of endophytic fungal media for inoculating wheat seeds
f) Soaking of wheat seeds for inoculation of selected endophytes
g) Re-isolation and identification of fungal endophytes from inoculated wheat
plants for confirmation of Koch’s postulate
h) Data collection regarding growth parameters
i) Statistical analysis
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CHAPTER 2 REVIEW OF LITERATURE
2.1 Origin and geographical significance of wheat
Wheat (Triticum aestivum L.) is very important crop for the huge population of
the world. It has been remained as first domesticated and essential staple food crop for the
key civilizations of North Africa, West Asia and Europe for last 10,000 years. The history
of wheat and history of human culture have co-evolved and co-existed, in a close
reciprocal relationship. Fertile Crescent is the part of the world (near and middle east) of
its earliest evolution and then its culture extended to all directions, from the Tigris-
Euphrates drainage basin (known as centre of wheat diversity) to entire world (Marcussen
et al., 2014).
Wheat is adapted to climatic conditions from latitudes of 30° and 60°N to 27° and
40°S; but cultivation in wide climate range commencing the Arctic Circle to the higher
elevations close to the equator can occur (Nutteson, 1957). CIMMYT reported that
production of wheat in warmer regions is technologically feasible. In altitude, it can be
cultivated from sea level to 3,000 m. The optimum cultivating temperature is 25°C, with
maximum and minimum growth temperatures of 30° to 32°C and 3° to 4°C, respectively.
It adapted to wide ranges of wet environment and might be cultivated in the major
localities having 250 to 1750 mm of precipitation range. Categorization into spring and
winter wheat is general and conventionally consider the season of the crop cultivation. In
winter wheat, stage of emergence of spike is delayed until a period of cold winter
temperature (0° to 5°C) experiences by the plant and the Spring wheat, the same as name
implies, is generally cultivated during spring (during autumn season in countries i.e.
Pakistan experience the mild winter season) and matures in summer (Marcussen et al.,
2014).
2.2 Economic importance and taxonomic status of the wheat
The grass family Poaceae (Gramineae) comprises most important crops for
d= days between two consecutive records (time intervals)y1 + yk = Sum of the first and last disease recordsy2 + y3 + - - - - - + yk-1= Sum of all in between disease scores3.8.11 Coefficient of Infection (CI)
Calculated the coefficient of infection (CI) by multiplying value of severity by 0.2, 0.4,
0.6, 0.8, 0.9 or 1.00 for host response ratings of resistant (R), moderately resistant (MR),
moderately susceptible (MS) or susceptible (S) respectively (Pathan and Park, 2006) to
categorize wheat genotypes into different groups.
3.9 Optimization of efficient and compatible endophytes with wheat seed
3.9.1 Collection of samples for endophytes
The samples of healthy leaves, roots and stems were taken from the desert plants
from various locations of Cholistan, Thar and Rohi Deserts. Samples were taken at
random from 3 to 5 healthy plants per site. The zip-lock bags were used for samples and
after that stored in ice buckets and were shifted to the lab, stored in refrigerator and were
used for isolation of endophytes within 72 hours. Samples were cleaned and washed until
yet soil removed, and then their surfaces were sterilized in 1 % (v/v) sodium hypochlorite
solution for 3 times and with distilled water.
35
By means of aseptic technique, 2-3 cm pieces of leaves, roots, and stems placed
on 10% PDA in petri plates and after that incubated at 28°C for 6-8 days to let the
emergence of fungi. Pure culture was obtained by the sub culturing of isolated fungi.
3.9.2 Morphological identification and mass culturing of endophytes
Fungal identification methods were based on the morphological characteristics of
their colonies (Najjar, 2007). The shape and size of conidia and phailides were calculated
and also compared the micro and macro morphological features to the identification key
(Hanlin, 1990; Barnett and Hunter, 1998; Pitt and Hocking, 2009) and after that pure
culture were multiplied.
3.9.3 In-vitro evaluation of endophytes
Spores of endophytic fungi were harvested in distilled water by rubbing the
surface of a sporulating pure culture with a sterile bent glass rod. Spore densities were
estimated using a hemocytometer and compound microscope (200x total magnification).
The spore suspensions were diluted in distilled water to prepare 105-106 spore mL-1.
Germinating wheat seed were kept in test tubes containing 0.3% agar concentration in
distilled water with fungal spore suspension of known concentration and were incubated.
After suitable intervals root and shoot length were measured and the efficacy of
endophytes were tested.
3.10 Field appraisal of selected efficient and compatible endophytes against drought and rust diseases
Seeds of two selected (from screening experiments) drought sensitive, leaf and
yellow rust susceptible genotypes of wheat each were soak in different selected (from lab
experiments) efficient and compatible endophytic spore suspensions for 24 hours and
then were sown in field with three replications and measured the antagonistic effect of
endophytes for enhancing the yield by reducing the disease severity as well as symbiotic
effect for tolerance of terminal drought. The parameters of Final disease severity (FDS),
AUDPC value, 1000-grain weight, Grain yield and Percent yield increased were
measured in case of leaf and yellow rust whereas 1000-grain weight, Number of
productive tillers, Biological yield, Grain yield and Percent yield increased were
measured in case of drought for assessing the role of fungal endophytes in stressed
environments. The endophytes were re-isolated from the inoculated plants to confirm the
colonization of the fungus in plant tissues. Re-isolation and identification of fungal
36
endophytes from inoculated wheat plants were done for the confirmation of their
existence.
3.11 Statistical analysis
Data were analysed using analysis of variance (ANOVA) and Dunkun’s New
Multiple Range Test (DNMRT), Tukey’s test at 5% probability level in screening
experiment and Least Significant Difference (LSD) test for other experiment (Steel et al.,
1997).
37
CHAPTER 4 RESULTS AND DISCUSSIONS
4.1: Response of different wheat genotypes against drought stress
4.1.1 Number of grains per spike:
While assessing the growth behaviour of wheat genotypes a decline was seen in
all growth parameters with escalating the drought conditions. Number of grains per spike
is an imperative yield interposing attribute for achieving high yield. Greater number of
grains per spike confirm high final yield. Data analysis of number of grains per spike is
the evidence for a considerable effect of imposed drought at the flowering and grain
filling stage on the number of grains per spike of different wheat genotypes during the
screening of 50 genotypes for assessing and screening of most effected genotypes by the
drought. Results showed highly significant (P≤0.001) effects among investigated wheat
genotypes for number of grains per spike in drought and normal conditions (Table 4.2).
The data concerning the number of grains per spike during 2014-15 year revealed
significant impact of drought stress on plants for this yield related parameter. In normal
water conditions, plants produced maximum grains per spike, while the imposed drought
stress significantly reduced the number of grains per spike.
A perusal of the table 4.1 showed the range of the number of grains per spike
among 50 wheat genotypes from 36 (Punjab-2011, Hashim-2010) to 49 (Millat-11, MH-
97) under normal conditions while under drought conditions the range for number of
grains was observed as 32.4 (Punjab-2011, Hashim-2010) to 46.6 (MH-97).
Under both normal and stress conditions, Hashim-10, Punjab-11, Watan-92,
Faisalabad-85 and Shafaq-06 were the genotypes which showed low number of grains per
spike while the genotypes Faisalabad-08, Uqab-00, MH-97, 9444, Pirsabak-04,
Faisalabad-83 Kohistan-97, Chakwal-50, Fareed-06 and Punjab-85 showed high number
of grains. Genotypes Punjab-85, 9495, Pothohar-73, Kohsar-95, Kohenoor-83 and
Parwaz-94 showed high number of grains in normal condition but produced low number
of grains per spike in drought condition, thus higher loss of number of grains was
depicted (Table 4.1).
Similar results were found by Bayoumi et al. (2008) who reported drought stress
resulted reductions in number of grains per spike and other yield components. Such
observations reported previously by Chandler and Singh (2008) and later by Dorostkar et
38
al. (2015). Differences in results may be because of the difference in circumstances in
which experiments were carried out.
4.1.2 1000-grains weight (g):It is one of the imperative yield contributing attribute in getting greater yield and
contains a pivotal character in restrictive yield potential of a genotype. 1000-grain weight
depends upon seed size. Greater the size of grain, higher will be the grain weight. The
analysed data of TGW of wheat exhibited a significant impact of terminal drought on
grain weight of different wheat genotypes during the screening of genotypes for assessing
and evaluating of most effected genotypes under drought. Results showed highly
significant (P≤0.001) effects among investigated wheat varieties for grains weight in
normal and drought conditions (Table 4.2). In normal water conditions, plants depicted
higher 1000 grain weight, while the drought stress significantly reduced it.
Results for 1000 grains weight during 2014–2015, showed that the highest grains
weight belonged to the genotypes Kohenoor-83 (44.79g) and the lowest related to
Hashim-2010 (35.25g) in normal conditions. In drought conditions, Millat-11 (42.1g) and
Mean 7.17B 9.41ALSD at 5% E=1.1970,V=0.7570 E*V= 1.6928
4.7 Discussion:Wheat crop production and yield is lower than its actual capacity because its
physiology is interrupted by many abiotic and biotic factors (Jellis, 2009). Among biotic
factors, diseases badly affect wheat yield in which rusts have caused huge yield losses in
recent years. Wheat rusts are prevalent throughout the world and its new races are evolving
day by day and infecting resistant varieties (Brian, 2006). Yellow and leaf rusts are presently
the imperative wheat disease worldwide, which threaten the global food security. There are
many reports about social and economic losses due to wheat rust epidemics (Hovmoller et al.,
2010).
Drought is one of the foremost abiotic stresses (Ramachandra et al., 2004; Boubacar,
2012) which cause low wheat productivity. Drought reduces the number of fertile tillers
which are main contributors of grain yield (Pfeiffer et al., 2005). It deters cell enlargement
and cell division and also reduces nutrient metabolism, respiration, photosynthesis and
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translocation (Farooq et al., 2008). Water stress disturbs plant water relations, minimizes
photosynthesis and plant energy results in death of the plant (Jaleel et al., 2007; Cattivelli et
al., 2008; Sikuku et al., 2012). Drought affects all of the wheat phonological stages, the
grain-filling and the reproductive wheat stages are the most sensitive (Pradhan et al., 2012;
Nawaz et al., 2013). Drought at post-anthesis reduces the wheat yield from 1-30%, mild
stress at heading stage losses 57% yield, whereas persistent terminal drought shrinks the grain
yield by 58–92% (Wei et al., 2010; Madani et al., 2010; Dias de Oliveria et al., 2013).
The productivity of wheat is enhanced by adopting appropriate strategies which
consequently minimizes severe yield losses caused by different abiotic stresses and
pathogenic diseases. Numerous scientists and researchers are discovering sustainable
alternative approaches to pesticides and chemical fertilizers. Natural resources are decreasing
with the passage of time due to spontaneously increasing world population. It is need of the
hour to find out an alternative approach for growing more food in such a manner that can
reduce detrimental environmental impacts of intensive farming, fungicide resistance and
environmental pollution.
The present research was conducted on endophytes, drought and rust diseases
tolerance in wheat. The endophytic beneficial effects on plants against diseases increased the
attention of researchers and farmers for enhancing agricultural production. This bio-control
strategy for combating different a biotic stresses and pathogenic diseases have altered the
attention of farmers for better crop production. It is tried to discover different efficient and
compatible fungal endophytes for wheat tolerance against drought and rust diseases.
Endophytes are metabolically active microbes (fungi, bacteria or virus) that colonise healthy
plant tissue intracellularly and intercellularly without causing any obvious disease symptoms
(Schulz and Boyle, 2006; Compant et al., 2008; Reinhold-Hurek and Hurek, 2011). They
exhibit complex interactions and a variety of symbiotic lifestyles with their hosts ranging
from parasitism to mutualism (Schulz and Boyle, 2005; Redman et al., 2001).
Endophytic microorganisms induce defence mechanisms in host plants against
pathogen attack. Plants combat different abiotic stresses by their own natural defence and in
cooperation with different microbes (Marulanda et al., 2006; Hardoim et al., 2015). In several
cases endophytic microbes produce bioactive organic compounds, secondary and
antimicrobial metabolites that resist pathogens (Clarke et al., 2006; Ambrose and Belanger,
2012; Gond et al., 2014). Several endophytic microbes also create tolerance in host plants
against abiotic stresses (Redman et al., 2002; Kuldau and Bacon, 2008). Endophytes are also
playing their imperative role for mutual interaction with their hosts for better adaptability and
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systemic resistance, augmenting nutrient uptake, stress tolerance and pathogenic tolerance or
resistance. The constructive and valuable characteristics of endophytic fungi have also
observed in host plants against numerous stresses (Hamilton et al., 2010; Kavamura et al.,
2013).
During the cropping season 2015-16 studies regarding symbiotic and synergetic
relationship of four selected fungal endophytes with two drought sensitive genotypes were
conducted on the wheat at the flowering and grain-filling stage. Results revealed that fungal
endophytes and genotypes significantly affected the grain yield and other yield related
parameters. Symbiotic effect of endophytes considerably contributed for alleviating drought
conditions through enhancing number of productive tillers, 1000-grains weight, biological
yield and finally grain yield of the crop. Piriformospora indica exhibited comparatively
significant response among the four fungal endophytes. Colletotrichum lindemuthianum also
showed better performance to combat the terminal drought conditions while interacting with
the sensitive wheat genotypes of Parwaz-94 and Kohsar-95 and increased 11.3% of final
grain yield after P. indica which gave 15.4% grain yield increase as compare to control
conditions while all other agronomic requirements were provided equally. Trichoderma
viride and Acremonium lolii also showed moderate response and 8.1% and 7.5% increase in
grain yield, respectively. The results of current research are also in line with the findings of
Shahabivand et al., (2012) and Yaghoubian et al., (2014) who reported that Piriformospora
indica enhanced wheat growth and its inoculation augmented the defence mechanisms in
wheat, conferred drought tolerance and increased yield and productivity of wheat plants,
suggesting P. indica application was playing its beneficial role by establishing interaction
with its host. Results are also consistent with Rodriguez et al., (2008) and Suryanarayanan et
al., (2009) who reported symbiotic and synergetic benefits conferred by Colletotrichum
lindemuthianum in tomato plants by improved drought tolerance, and also enhanced growth
and biomass of host.
In the same cropping season 2015-16, studies were also carried out related to the
exploring the symbiotic and synergetic relationship of four selected fungal endophytes with
two leaf rust susceptible genotypes Faisalabad-85 and Aas-02 and two yellow rust susceptible
genotypes namely Fareed-06 and Shafaq-06 for stabilizing wheat plant under artificial and
natural inoculation environments. The artificial inoculation of yellow and leaf rusts was
performed on wheat genotypes by means of different methods like rubbing, dusting through
talcum powder, spraying with distilled water and needle injection methods. The same studies
concerning artificial inoculation conducted by Hussain et al., 2015; Rao et al., 1989 using
89
same method of hypodermic injection through an aqueous spore’s suspension. Dusting and
spraying methods used by Roelfs et al., 1992 who mixed fresh spores in talcum powder and
distilled water and followed by applied to wheat plants.
It is evident from the results that symbiotic effect of fungal endophytes significantly
contributed for alleviating pathogenic leaf and yellow rust conditions through minimizing
both of the final rust severities (FDS) and AUDPC values and via enhancing 1000-grain
weight and wheat grain yield by comparing with control while all other agronomic
requirements were provided equally. Piriformospora indica and Trichoderma viride were
performed significant among the four endophytes to confront the disease conditions while
interacting with the leaf and yellow rust susceptible wheat genotypes. Both reduced the leaf
rust severities by 40% and 30% and also yellow rust severities 40% and 30%. Thus, final
grain yield were increased 17.5% and 13.7% against leaf rust whereas 12% and 10% against
yellow rusts. Colletotrichum lindemuthianum and Acremonium lolii showed moderate
performance.
The findings of present research are similar with the results of Rabiey and Shaw
(2015) who reported that P. indica was helpful in biological control of Fusarium wheat
diseases. Assessment was done for the antagonistic and biocontrol effect of P. indica on
fusarium head blight (FHB) disease of spring and winter wheat. Fusarium head blight caused
by the contamination of the mycotoxin deoxynivalenol (DON). Application of P. indica
reduced 70% of disease incidence and severity and reduced 70 and 80% concentration of
mycotoxin deoxynivalenol in winter and spring wheat respectively. P. indica also increased
1000-grains weight, biological and grain yield. The average increase of biological and grain
yield were reported 24.2 % and 17.3 %.
The results are also in consistent in case of antagonistic effect of P. indica by Rabiey
et al., (2015) for control of air-borne diseases of spring and winter wheat, including yellow
rust, powdery mildew and septoria leaf blotch in outdoor conditions. The host genotypes
were inoculated naturally and artificially with corresponding pathogens of air-borne diseases.
Application of P. indica at sowing time reduced the disease severities of yellow rust,
powdery mildew and septoria leaf blotch by 29, 63 and 65% respectively. Consequently, it
also increased 1000-grain weight, biological and grain yield by 25, 48 and 27 % respectively.
The performance of Piriformospora indica was also evaluated by Rabiey et al.,
(2015) for control of Fusarium crown rot of wheat which caused decrease in straw production
as well as grain quality and grain yield. Wheat seedlings were inoculated with P. indica and
pathogenic Fusarium culmorum at sowing time and growth of 7 days were checked under
90
glasshouse conditions. Seedlings without inoculation of P. indica were badly damaged by F.
culmorum pathogen but root seedlings inoculated with P. indica and F. culmorum were not
damaged.
Serfling et al., (2007) reported the effect of P. indica in different substrata under field
and greenhouse conditions by colonizing winter wheat roots with this biocontrol endophyte
against different root, stem and leaf pathogens. In greenhouse conditions, severity of typical
root (Fusarium culmorum), stem (Pseudocercosporella herpotrichoides) and leaf (Blumeria
graminis f. sp. tritici) pathogens were reduced significantly. However, in field conditions,
symptoms of leaf pathogen were not significant in Piriformospora indica colonized
compared with control. But the stem pathogen disease severity of Pseudocercosporella
herpotrichoides was much reduced in endophytic colonized plants. Enlarged concentrations
of hydrogen peroxide and numbers of sheath layers after B. graminis attack were detected in
endophytic colonized plants that means systemic resistance induction was done in plants.
Results are also consistent with Montero-Barrientos et al., (2010), Shoresh et al.,
(2010) and Mastouri et al., (2010) who reported antagonistic effect conferred by Trichoderma
viride in many of the host plants. For that reason it considered as bio-control fungi for their
ability to manage diseases. Trichoderma as biocontrol agents catch the attention for
managing diversity of soil borne fungi of Sclerotiorum cepivorum, Botrytis allii and
Aspergillus niger which are the causal organisms of neck rot black mould and white rot
disease of onion, respectively (Metcalf et al., 2004; Clarkson et al., 2004; McLean et al.,
2005). It is reported valuable in protecting Arachis hypogaea, Cucumis sativus and a number
of other crops from destruction caused by several pathogens (Ha, 2010).
P. indica confront fungal root pathogens such as Fusarium spp., Rhizoctonia solani
and Cochliobolus sativus and protect barley plants from their deleterious effects (Waller et
al., 2005). Additionally, protection of systemic type against foliar pathogens is achieved
which is a beneficial effect connected to the mutualistic interaction. Generally, systemic
resistance show a defence approach by hosts to check microbes’ invasions to infection sites,
thus, to defend yet uninfected organs of host. However, in case of barley, Piriformospora
indica activates plant defence responses that ultimately direct a systemic resistance against
Blumeria graminis f.sp. hordei (Waller et al., 2005).
The frequently observed quality of improved stress tolerance in colonized host plants
of P. indica was also reflected in barley and Arabidopsis by an increased salt tolerance and
the systemic resistance induction against the powdery mildew fungi Golovinomyces orontii
and Blumeria graminis f.sp. hordei (Waller et al.,2005). It is extensively reported that
91
infestation by P. indica spores and culture filtrates leads to improvement of the growth,
increase in root and biological yield in its mutualistic relationship with a broad range of hosts
(Achatz et al., 2010; Zarea et al., 2012; Jogawat et al. ,2013; Bakshi et al., 2014) increase in
grain yield, enhanced nitrate and phosphate uptake (Yadav et al., 2010; Cruz et al., 2013;
Shrivastava and Varma, 2014) and enhanced tolerance to major biotic and abiotic stresses
under glasshouse and field conditions (Ghahfarokhy et al., 2011; Alikhani et al., 2014;
Ghabooli et al., 2014; Varma et al., 2014; Harrach et al., 2014; Prasad et al., 2014; Johnson
et al., 2014; Trivedi et al., 2016; Gill et al., 2016).
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CHAPTER 5 SUMMARY
Wheat production and yield is much low in Pakistan due to numerous abiotic and
biotic factors in which drought, leaf and stripe rusts are very important. Leaf rust/brown rust
is caused by the Puccinia recondita yellow rust/stripe rust is caused by Puccinia striformis.
These pathogens spread through air as well as these are persistent threat for sustainable wheat
productivity.
To combat these threats for food security, it is necessary to discover alternative
sustainable and environment friendly approaches. Therefore, during 2014-15 and 2015-16,
the research was conducted to confirm the hypothesis that endophytes confer drought and rust
diseases tolerance in wheat genotypes. During 2014-15, fifty genotypes were screened to find
out drought sensitive, leaf and yellow rusts susceptible genotypes in 3 separate screening
experiments. The rust conditions were produced by providing artificial inoculation of yellow
and leaf rust at tillering and heading stage on wheat genotypes by means of various methods
like dusting with talcum powder, spraying with distilled water and needle injection. Drought
conditions were provided by skipping the irrigation at reproductive and grain filling stage.
In screening experiment, the mean comparisons of yield parameters and drought stress
related indices such as tolerance index, mean productivity and stress susceptibility index of
wheat exhibited a significant impact of terminal drought on the number of grains per spike,
1000-grain weight, number of productive tillers, harvest index, biological yield and finally
grain yield. Based on mean comparisons, the genotypes were categorized into four groups;
i. The genotypes of 9725, Millat-11, Inqalab-91, 9444, Lasani-06, Manthar-03,
Pirsabak-04, MH-97, Kohistan-97 and Faisalabad-83 expressed less grain yield losses
as well as high yield in both drought and normal conditions.
ii. The genotypes of Hashim-10 and Punjab-11, Watan-92, GA-02, Faisalabad-85,
Shafaq-06 and Aas-02 showed minimum grain yield than first group in both drought
and normal conditions.
iii. Chenab-00, Kohsar-95, Parwaz-94 and Kohenoor-83 genotypes of wheat expressed
high grain yield under normal condition and low grain yield under drought condition.
Genotypes of this group confirmed higher loss of grain yield due to drought stress.
Similarly, it was also observed that genotypes belong to this group are most sensitive
to drought.
iv. Likewise, the rest of the genotypes are included in the fourth group.
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In the second screening experiment, the mean comparisons of different disease
parameters of final disease severity % (FDS), AUDPC and coefficients of infection (CI)
exhibited a significant impact of leaf rust on 50 wheat genotypes. On the basis of above
mentioned disease parameters, the genotypes were classified into four categories: a) S-
susceptible b) MS-moderately susceptible c) MR-moderately resistant d) R-resistant. The
genotypes namely Punjab-11, Faisalabad-85, Aas-02, Sehar-06 and Wafaq-01 expressed
susceptible response whereas Manthar-03, Parwaz-94, Bathoor-08 and few among the rest
genotypes showed resistant response.
Similarly, in further screening trial Fareed-06, MH-97, Shafaq-06, Inqalab-91 and
Aas-02 exhibited susceptible response whereas Bhakhar-02 and Fsd-08expressed resistant
response. In in-vitro evaluation endophytes were conducted by keeping the seeds in test tubes
containing 0.3% agar concentration in distilled water with endophytic fungal spore
suspension of known concentration. The efficacy of endophytes was tested by measuring the
root and shoot length of wheat seedlings. Four efficient endophytes namely Piriformospora
indica, Colletotrichum lindemuthianum, Trichoderma viride and Acremonium lolii were
selected among them for further studies.
During 2015-16, three experiments were conducted to investigate the symbiotic
relationship of four selected endophytes for stabilizing wheat plant under drought, leaf and
yellow rust conditions respectively. The drought sensitive genotypes like Kohsar-95 and
Parwaz-94 showed significant results along with endophytes. Endophytes enhanced the
number of productive tillers, 1000-grains weight, grain and biological yield of endophytic
inoculated drought sensitive genotypes in drought stress conditions as compare to control.
Piriformospora indica showed significant performance by enhancing 15.4% final grain yield
followed by Colletotrichum lindemuthianum (11.3 %), Trichoderma viride (8.1 %) and
Acremonium lolii (7.5 %) respectively.
In case of leaf and yellow rust conditions, the leaf rust susceptible genotypes namely
Faisalabad-85 and Aas-02 and the yellow rust susceptible genotypes namely Fareed-06 and
Shafaq-06 showed significant results with fungal endophytes. Endophytes enhanced 1000-
grains weight and grain yield by reducing the disease severity and AUDPC values of those
endophytic inoculated rust susceptible genotypes in disease conditions as compare to control.
Piriformospora indica also showed significant performance in cases of leaf and yellow rust
diseases by enhancing 17.5% and 12.3% final grain yield followed by Trichoderma viride
which showed 13.7 % and 10.6 % in leaf and yellow rust conditions respectively. The rest of
94
endophytes Colletotrichum lindemuthianum and Acremonium lolii showed 7.1% and 6.2%,
8.2% and 4.2% in leaf and yellow rust conditions respectively.
CONCLUSION: Environmental factors strengthen the wheat by confront abiotic and biotic stresses in
combination with symbiosis.
Endophytes confer the drought and rust diseases tolerance in wheat genotypes.
Endophytes can protect wheat from damage caused by Puccinia recondita and Puccinia
striiformis by reducing the disease severity and consequently enhance the grain yield
under field conditions.
Piriformospora indica showed best performance against drought and rust diseases.
Trichoderma viride exhibited outstanding performance against rust diseases under field
conditions.
Colletotrichum lindemuthianum showed significant performance against drought stress
under field trials.
RECOMMENDATIONS: It is strongly recommended that endophytes should utilize against drought and rust
diseases under favorable environmental conditions.
Wheat seeds should be treated with Piriformospora indica to get maximum yield under
rust favorable and water deficient conditions.
Wheat seeds treated with Colletotrichum lindemuthianum is most suitable to get good
yield from deficient water environment.
Maximum wheat yield was obtained when seeds were treated with Trichoderma viride
against rust diseases.
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