1.
INTRODUCTION
Maize lethal necrosis
(MLN) is a disease currently affecting corn (Zea mays) production in East and Central Africa (Mahuku
et al., 2015a, 2015b; Wangai et al., 2012; Adams et
al., 2013, 2014; Lukanda et al., 2014). MLN is caused
by combined infection of Maize chlorotic mottle virus
(MCMV) and any maize infecting virus in the Potyviridae family such as Wheat
streak mosaic virus (WSMV), Maize dwarf mosaic virus (MDMV) and Sugarcane mosaic
virus (SCMV) (Niblett & Claflin
1978; Uyemoto et al., 1980). In East Africa the
primary cause of the disease is co- infection with Maize chlorotic
mottle virus and Sugarcane mosaic virus (Wangai et
al., 2012; Adams et al., 2014; Lukanda et al., 2014; Mahuku et al., 2015).
A survey carried out
in East African countries to study the distribution of MLN causing viruses
suggested up to 94% incidence in randomly selected symptomatic plants (Mahuku et al., 2015). Tanzanian samples collected at Arusha and Mwanza had 60% to 69%
incidence and both viruses were detected (Mahuku et
al., 2015). The survey indicated wide distribution and high prevalence of MLN
viruses in East and Central Africa.
MLN causes chlorotic mottling from the plant base, leaf necrosis from
the margins to the midrib, stunted plant growth, premature death, male
sterility and failure to tassel, malformed ears or lack of ear formation, and
rotten or small cobs with little or no grain fill (Niblett
& Claflin, 1978; Wangai
et al., 2012). The magnitude of yield loss associated with the disease makes
developing cultivars with disease resistance crucial. In Kenya, MLN caused an
estimated loss of $187 million equivalent to $364/ton in 2012 (De Groote et
al., 2016). Farmers in MLN areas have experienced a significant decrease in yield
since MLN was first reported in 2010 (Makone et al.,
2014).
Potyviruses are endemic to East
Africa and were observed to cause crop loss of 18% to 46% (Louie, 1980). The
introduction of MCMV and co-infection of maize with the endemic potyviruses to cause MLN represents a new threat to maize
production in East African countries (Wangai et al.,
2012). There is a need for
identification of MLN resistance sources, mapping of genomic regions with MLN
resistance and intogression of resistance genes into
widely used susceptible inbred lines and hybrids in East Africa (Semagn et al., 2015). The study evaluated Recombinant
Inbred Lines (RIL) with potyvirus resistance QTL in
disease hotspots in Tanzania and under high disease pressure through artificial
inoculation in the growth chamber and field. The RIL population is derived from
multi-virus resistant parent Oh1VI and a susceptible parent Oh 28. The population
was genotypically analyzed for
potyvirus resistance and QTL for potyvirus
resistance were mapped to chromosome 3, 6 and 10 (Zambrano
et al., 2014). Selected lines with combinations of the QTL were used to analyse
the influence of potyvirus resistance in MLN control.
The study aimed to fill the knowledge gap concerning the influence of potyvirus resistance QTL for the control of MLN and the
suitability of temperate lines in managing MLN in Africa.
2.
MATERIALS AND METHODS
2.1
Plant
materials
Inbred lines selected
from a Recombinant Inbred line (RIL) population derived from a multi-virus
resistant parent Oh1VI and susceptible parent Oh28 were used for the study. The RIL population was generated by the Corn,
Soybean and Wheat Quality Research Unit (CSWQRU) at the Ohio Agricultural
Research and Development Centre (OARDC). The RIL population was previously
genotyped with 768 single nucleotide polymorphism (SNP) markers and QTL for potyvirus resistance (Zambrano et
al., 2014). Selections were based on
molecular markers flanking QTL for potyvirus
resistance on chromosomes 3, 6 and 10 alone and in all possible combinations.
Flanking markers PHM13823-7 and PZA00667-1 were used to select for chromosome 3
QTL, markers PHM15961-13 and PZA00540-3 selected chromosome 6 QTL and flanking
markers PHM1812-32 and PHM15868-5 selected chromosome 10. Five independently
chosen lines represented one individual QTL or a combination QTL from
chromosome 3, 6 and 10. Lines 80231, 80229, 80209, 80221 and 80196 had allele
for resistance on chromosome 3, 6 and 10 forming a treatment group of 3_ 6_10.
Genotypes were
planted for evaluation in a growth chamber at the Department of Plant
Pathology, Ohio State University/OARDC, Wooster, Ohio, May to July 2015 and at
the CYMMIT – KALRO MLN Screening Facility, Naivasha,
Kenya in December 2015 to March 2016. In natural infection trials treatments
were planted for evaluation in fields at Babati – Manyara (latitude: -4.20963602, longitude: 35.73990726,
elevation: 1378m) and Mlangalini – Arusha (latitude: -3.3666700, longitude 36.6833300,
elevation 1415m), Tanzania during the rain seasons of 2015 and 2016.
In all experiments
except for the field inoculation and 1st natural infestation
experiment, both parents were included as resistant and susceptible controls
and to provide baseline information on disease incidence and severity on each
experiment. Control lines 80066 and 80293 from Oh1VI RIL population which lack
resistance alleles on all three chromosomes were included in a growth chamber
experiment and CML444 and entry73 tropical lines from CIMMYT were included as
controls in a field inoculation experiment as susceptible local controls and local checks CML144,
CML197, CML442, CML395, KS23-6 and KS23-5 were
used in a natural infection experiment.
2.2
Viral
inoculum sources
The isolates of SCMV
and MCMV used for a growth chamber experiment were maintained by the USDA,
CWSQRU. The SCMV-OH isolate was
collected from Ohio (Louie, 1986) and the MCMV-KS isolate was collected from
Kansas (Niblett & Claflin,
1978). The sequence of MCMV-KS is 96%-97% identical to the East African isolate
which is 98%-99% identical to isolates from China (Mahuku
et al., 2015). The SCMV-OH isolate was maintained by serial mechanical
transmission to a susceptible maize line, and the MCMV-KS isolate was stored
frozen and in liquid nitrogen and transmitted to the susceptible line Oh28 as a
source of inoculum. Presence of the
viruses in symptomatic plants was confirmed by tissue blot immunoassay as
previously described (Jones et al., 2011).
Inoculum made from a mixture of infected leaf tissues for both viruses
was prepared in a combination of 1:4 MCMV to SCMV to attain uniform MLN pressure.
Inoculum was prepared by grinding symptomatic leaf tissues in a 0.1 M potassium
phosphate in 1:10 dilution ratio (1 gram of tissue to 10 milliliters
of the 0.1M, 7.0 pH potassium phosphate buffers) using mortar and pestle. Carborundum (0.02 g/ml) was added as an abrasive agent. The
prepared inoculum was rub inoculated to leaves of 14 days old seedlings (Jones
et al., 2007). There were two inoculations per experiment with the second
inoculation applied two days after the first to ensure successful infection.
Plants were transferred to a growth chamber with a 25-21oC
(day-night), 75% relative humidity, 532 µmol light
intensity (microeinsteins) and a 12 hr photoperiod.
In
a field inoculation experiment the inoculum was prepared following the protocol
used at the MLN screening facility at Naivasha under
CIMMYT and KARLO using East African isolates of SCMV and MCMV maintained
through serial transmission to susceptible maize (Gowda
et al., 2015). The inoculum was made from a mixture of symptomatic tissues with
individual infection of SCMV and MCMV in a combination of 4:1 ratio
respectively. The inoculum was prepared by harvesting the plants infected with
SCMV and MCMV separately, and then leaves were chopped, weighed and blended in
0.1M potassium phosphate buffer with 1:20 dilution ratio (leaf material:
buffer) at a pH of 7.0 and sieved to remove plant debris. The inoculum was
mixed in a larger tank and Carborundum 1g/liter was added. Field inoculation was done using a
motorized mist blower (Solo423 MistBlower, 11 liter capacity). The inoculum was delivered at a pressure
of 10 kg/cm2 with a 2-inch nozzle. Inoculation was carried out at
the 4-6 leaf stage and repeated after one week.
2.3
Experimental
design
All experiments were
established following the alpha lattice design. Except for trial 4 under
natural infection all experiments were arranged in an alpha lattice design of
42 treatments in 3 replications; each replication consisted of 6 blocks with 7 treatments
each. Trial 4 had a total of 40 treatments and each replication had 4 blocks of
10 treatments. Each treatment was planted in a row of 5m with intra-row spacing
of 25 cm and inter-row spacing 75 cm. All trials were planted under rainfed conditions; irrigation was supplementary in
non-rain days and Diammonium phosphate (DAP) was
added at planting and UREA as a top dressing to supplement nitrogen and
phosphorus sources using local recommended rates.
2.4 Data collection
For the growth
chamber experiment plants were evaluated for disease development beginning 7
days post second inoculation and rating continued every four days until 23 days
post inoculation. For the field inoculation experiment disease rating was done
2 weeks post inoculation continuing every 7 days until 42 days post inoculation
and for natural infection disease severity ratings were initially performed
every seven days and then extended to 14 days covering a total of 56 days.
Disease was scored on a scale of 1 to 5 as follows: 1 = no visible MLN
symptoms, 2 = fine chlorotic streaks mostly on older
leaves, 3 = chlorotic mottling throughout the plant,
4 = excessive chlorotic mottling on lower leaves and
necrosis of newly emerging leaves (dead heart), and 5 = complete plant necrosis
(Gowda et al, 2015). Severity scores collected were
used to generate area under the disease progress curve (AUDPC) values. The
equation for AUDPC is
where; Yi is disease
assessment (score), at the ith
observation, ti is the time of observation (days) at
the ith observation and n is the total
number of observation. First scores, last scores mean scores and AUDPC values
were used to test for differences among treatments.
Analysis was done
using the R package version 3.1.1(R Development Core team, 2014). The Agricolae package version 1.2-3 (de Mendiburu,
2010) was used to test for differences among treatments in measured parameters.
The experimental model for the alpha lattice was Yij
= µ (Mean effect) + Ɍi (Replicate) +Ƭj
(Treatment effect) + βi (Incomplete Block effect) +Ɛij
(Intra –block error effect). The PIBI.test function was used for the partial incomplete block
design to correct for incomplete block effects (de Mendiburu,
2010). A two-tiered analysis was conducted in which the adjusted means from the
alpha-lattice were then used to test the null hypothesis that there are no
differences between higher order QTL treatments when comparing 3, 6, and 10
alone; 3 and 6, 3 and 10, 6 and 10, in combinations; and 3, 6 and 10 together.
The later model was then tested using a general linear model in the R core
package version 3.1.1(R Development Core team, 2014). Since different checks
were used in different experiments, each experiment was analysed differently
and all the treatments were normalized to a susceptible check Oh28.
3.
RESULTS
In the growth
chamber, there was significant variation among genotypes and among different
combinations of potyvirus resistance QTL to MLN
inoculation. Genotypes with combinations of resistance QTL groups from
chromosome 3, 6 and 10 developed less disease symptoms compared to genotypes
with single resistance QTL (Table 1).
Under field
inoculation no significant differences in MLN symptoms expression was observed
between individual RIL genotypes and controls or for QTL groups. Field ratings
were conducted over an extended 42 days period, which may have affected our
ability to discern differences. The
analysis based on QTL groups indicates that genotypes with QTL combinations of
3 + 6 + 10 has significantly lower means and AUDPC scores compared to other
genotype groups. However, the adjusted means for first scores and last scores
were not significantly different in the field environment (Table 1).
There was no
significant variation among genotypes with different QTL combinations in trial
1 set at Mlangalini, Arusha,
Tanzania presumably due to low incidence. Significant variation (P = 0.05)
among QTL groups was observed in 3 experiments (trials 2 through 4) set at
Krishna seed farm and KIRU-6 village at Babati, Manyara, Tanzania in the first scores, last scores, mean
scores and AUDPC (Table 1).
4.
DISCUSSION
The study aimed to determine which of the three potyvirus resistance QTL on chromosome 3, 6 and 10 might
provide protection against MLN. No genotypes were unaffected by MLN, signifying
that the QTL under study were not providing immunity. The best performing
genotypes had a combination of potyvirus resistance
QTL on chromosomes 3, 6 and 10. These three QTL were previously shown to be
important in providing protection against SCMV (Zambrano
et al., 2014), MDMV (Jones et al., 2007) and WSMV (Stewart et al., 2012). The
potential role of two QTL interactions cannot be disregarded, as combinations
of QTL 3 + 6 and 3 + 10 were also significantly better than controls.
Resistance to potyvirus is
clustered in the maize genome (Redinbaugh &
Pratt, 2009). Loci on the short arm of chromosome 6 and near the centromere of
chromosome 3 have major effect on potyvirus
resistance (Jones et al., 2007; Redinbaugh et al.,
2004; Xia et al., 1999; Wang et al., 2003, Zhang et al., 2003; Zambrano et al., 2014).
The locus on chromosome 3 near the centromere at bin
3.04/3.05 in combination with other QTL confers resistance to many viruses
including WSMV, SCMV, MMV and MCDV (Redinbaugh & Zambrano, 2014). The locus overlaps the position of
translation factor eIF4e (Zambrano et al., 2014), involved
in conferring virus resistance by producing proteins, which fail to interact
with the virus (Gomez et al., 2009). Current studies on MLN resistance found
other candidate genes for resistance to MLN on the same region (Gowda et al., 2015; 2018). Other candidate genes include
those with a function predicted to restrict virus movement within the plant as
demonstrated in arabidopsis by Chrisholm
et al (2000). A locus on chromosome 3.05 is known to be responsible in plant defense against pathogens encodes nucleotide-binding site leucine-rich repeat (NBS-LRR) protein (Xiao et al., 2007).
Recently, the locus on chromosome 3 was identified among
for QTL responsible for MCMV resistance in the Oh1VI RIL population others
being the loci on chromosome 1, 2, and 10 (Jones et al., 2018). The study also denoted
that the locus on chromosome 3 was near marker S3_37246834 which had the LOD
score of 4.3 explaining 16% of the phenotypic variation and the locus on
chromosome 10, which was centred at marker S10_134058628, had the LOD score of
9.0 explaining 11% of the phenotypic variation. These loci overlap the same
region responsible for resistance to Potyvirus and
other multiple virus families as explained by Zambrano
et al. (2014). The identified locus
on chromosome 2 was unique to the Oh1VI population centered
on marker S2 _ 163825081 with a LOD score of 10 explaining 18% of phenotypic
variance (Jones et al., 2018). Other studies have also mapped the region on
chromosome 3 and 6 as potential candidate for marker assisted MLN resistance
breeding (Gowda et al., 2018). Other recent studies
have also suggested the need to focus improve resistance to both viruses
causing MLN than focusing on the disease itself (Karanja
et al., 2018).
Generally, results indicate the role of potyvirus resistance
in MLN control.
Although none of
the genotype were immune
to MLN there
is differences in
response of genotypes
and QTL to MLN
infection. Genotypes with all three potyvirus
resistance QTL on chromosome 3, 6 and 10 had more resistance to MLN than
genotypes with one of the above QTL. This
lead to a
conclusion that, there
is a role played by potyvirus resistance
in MLN control
especially in reducing
MLN effects. More studies are needed to know the exact
role played by potyvirus resistance and how much MLN
effects are reduced with the presence of potivirus
resistance QTL. This will provide the basis for introgressing
potyvirus resistance in East African maize germplasm and pave way for a holistic approach of
controlling MLN in Sub Saharan Africa.
In carrying out future studies, especially in field
conditions in East Africa, materials used should be adapted to tropical environment. The RIL
populations used for the
study were derived from
Oh1VI and Oh28 which originate from temperate
environment hence did
not perform well
in tropical environment. Agronomically, genotypes performed poorly compared to
tropical controls in parameter measured such as plant height, ear height, yield
and days to anthesis and silking.
The gap between anthesis and silking
was also big indicating materials were under physiological stress which
could hinder reproduction and the
plants were attacked by a
lot of
endemic disease such
as maize streak virus and a variety of insects and
vectors. This could affect the results and quality of the study especially when
disease scoring is done until plants have reached maturity.
Acknowledgement
We deeply appreciate the USAID feed the future program under iAGRI-Tanzania for funding our research work in US and
Tanzania and the Borlaug LEAP fellowship for funding the research work in
Kenya. Our sincere thanks also go to the USDA, ARS Corn, Soybean and Wheat
Quality Research Unit (CSWQRU) at Selby hall and Dr. Francis’ lab at Williams’s
hall, OARDC, Wooster for supporting lab and green house activities. Many thanks
also go to ARI-SELIAN in Arusha, Tanzania for their
supporting field trials in MLN hotspots at Babati and
to CIMMYT Kenya for their support in carrying out field inoculation experiments
at the MLN screening facility in Naivasha, Kenya.
Funding
This work was funded by the Innovative
Agriculture Research Initiative [iAGRI] project, 2014
- 2016 and Norman Borlaug Leadership Enhancement in Agriculture Program
[Borlaug LEAP] project, 2015 -2016.
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