Role of Lanc like G protein-coupled receptor-2with BOP and BTB/POZ in Stress Tolerance and High Yielding trait of Pigeonpea

Abstract

Pigeonpea is drought resilient crop; relatively more drought tolerant than other legume crops. Through detailed evaluation and multi-location trials of cross derivatives, we identified 65 better performing pigeonpea lines. Among these lines, high yielding and stress-tolerant accessions were identified. From our earlier MYB network and flowering genes networks, we could identify tightly linked co-expressinggenes for yield traits. Semi-quantitative expression analyses showed that the defending type drought stress tolerance contributing LAN C like protein GCL-2 is expressed in providing disease resistance and myb linked BTB/POZ genes contribute for high yielding of pigeonpea. BOP is a member of BTB group of plant protein. We found differential up-regulation of these genes in drought-tolerant high yielding pigeonpea lines earlier reported by our team. Whereas in another report we explained the myb linked expression of BTB/POZ genes. These genes selected from our earlier network analyses were identified, PCR amplified, sequenced and structure validated for its functional domain. Using the gene sequence, we predicted and validated the protein structure of Lan C. The current study extends our earlier findings that these genes are directly taking part in stress tolerance and high yielding traits.

Full text

Journal of AgriSearch, 6(3):105-112
1* 1 1
JESHIMA KHAN YASIN , SAKSHI CHAUDHARY , BHAIRAV NATH PRASAD ,
2 3 4
ARUMUGAM PILLAI , NIDHI VERMA AND ANIL KUMAR SINGH
ISSN : 2348-8808 (Print), 2348-8867 (Online)
https://doi.org/10.21921/jas.v6i03.16209
An Open Acc ess Intern ational Pee r Reviewed Quarterl y
Role of Lanc like G protein-coupled receptor-2with BOP and BTB/POZ
in Stress Tolerance and High Yielding trait of Pigeonpea
1Division of Genomic Resources, ICAR-National Bureau of Plant Genetic Resources, New Delhi, India
2Department of Plant Breeding and Genetics, Agricultural College and Research Institute, Tamil Nadu
Agricultural University, Killikulam, Vallanadu, Tamil Nadu, India
3 KAB, Indian Council of Agricultural Research, PUSA campus, New Delhi, India
4Division of Land & Water Management, ICAR-Research Complex for Eastern Region, Patna, Bihar, India
*Corresponding author email: Yasin.Jeshima@icar.gov.in
Pigeon pea is drought resilient crop;
relatively more drought tolerant than other
legume crops. Through detailed evaluation
and multi-location trials of cross derivatives,
we ide ntified 65 be tter pe rform in g
pigeonpea lines. Among these lines, high
yielding and stress-tolerant accessions were
identified. From our earlier MYB network
and flowering genes networks, we could
identify tightly linked co-expressinggenes
for yield traits. Semi-quantitative expression
analyses showed that the defending type
drought stress tolerance contributing LAN
C like protein GCL-2 is expressed in
providing disease resistance and myb linked
BTB/POZ genes contribute for high yielding
of pigeonpea. BOP is a member of BTB group
of plant protein. We found differential up-
regulation of these genes in drought-tolerant
high yielding pigeonpea lines earlier
reported by our team. Whereas in another
rep ort we ex plained the myb linked
expression of BTB/POZ genes. These genes
selected from our earlier network analyses
were identified, PCR amplified, sequenced
and structure validated for its functional
domain. Using the gene sequence, we
predicted and valida ted th e protein
structure of Lan C. The current study
extends our earlier findings that these genes
are directly taking part in stress tolerance
and high yielding traits.
Pigeonpea, stress, protein, LanC, gene
KEYWORDS
ABSTRACT
INTRODUCTION
105
P
Anonymous, 2014
igeonpea (Cajanus cajan) is one of the most common tropical and subtropical
legumes cultivated for its edible seeds. Pigeonpea is fast-growing, hardy,
widely adaptable, and drought-resistant ( ).Pigeonpea
can grow on a wide range of soils, from sands to heavy black clays, with variable
pH. However, the best pH range is within 5-7. It has a low tolerance of soil salinity,
but some cultivars were reported to tolerate high (6-12 dS/m) salinity ( ).
Because of its drought resistance, it can be considered of the utmost importance for
food security in regions where rainfall is unreliable and droughts are prone to occur
( ).The origin of pigeonpea (C. cajan) is either North-Eastern
Africa or India ( ). Its cultivation dates back at
least 3000 years ( ). It isa pantropical
and subtropical species particularly suited for rainfed agriculture in semi-arid
areas because of its deep taproot, heat tolerance and fast-growing habit
( ). Pigeonpea is present in both hemispheres, from 30°N to
30°S and from sea level to an altitude of 3000 m ( ). Though sensitive to
frost, pigeonpea keeps growing at temperatures close to 0°C and tall plants can
survive a light frost. It grows better where annual rainfall is above 625 mm.
However, it is highly tolerant of dry periods and, where the soil is deep and well-
structured, it continues growing with rainfall as low as 250 to 375 mm. Pigeonpea is
sensitive to water logging and salt spray. Under shade growth is reduced and bears
thin, pale green foliage and few pods ( .
Sudden climate changes and unavailability of sufficient water supply can severely
affect the productivity of agriculturally important crops. Additionally, frequent
exposure to environmental stresses such as drought is adversely affecting plant
growth and yield. Pigeonpea is cultivated in marginal lands with minimum
fertilizer and irrigation facilities making it more vulnerable to water stress during
growth and development.Even for short-duration varieties, the yield gets affected
due to water stress during early pod development and late flowering stages (
). During seed hardening, the crop requires a considerable amount of
water and at this crucial stage unavailability of water often causes terminal
drought. Despite having deeper roots, drought acts as major yield-limiting factors,
especially at critical seedling and reproductive stages of pigeonpea ( ).
The onset time, intensity and duration of drought stress can fluctuate during
plant growth and yield loss depends on it ( ). There has been
increased progress made in developing drought-tolerant pigeonpea genotypes,
but still, it is difficult to meet the conditions arisen due to climate change. It is
feasible to develop drought-tolerant varieties through genomics-assisted breeding
that would facilitate yield stability under water-deficient conditions (
).
As drought is controlled by multigenes, identification of candidate genes and
understanding the molecular mechanism associated with drought tolerance in
pigeonpea is critical. Many studies have been conducted in model plants to identify
candidate genes associated with drought response ( In pigeonpea,
genomics resources have been developed which can be deployed to identify
Bekele-Tessema, 2007
Duke, 1983
Van Der Maesen, 1989; Ecocrop, 2016
Van der Maesen, 1989; Mallikarjuna et al., 2011
Mallikarjuna et al., 2011
Ecocrop, 2016
FAO, 2016)
Lopez
et al., 1996
Saxena, 2008
Hu and Xiong, 2014
Varshney et
al., 2014
Mir et al., 2012).
ARTICLE INFO
Received on
Accepted on
Published online
20-12-2017
18-06-2019
01-09-2019
:
:
:

[Journal of AgriSearch, Vol.6, No.3]
Role of LanC in Stress and Yield trait of Pigeonpea
106
candidate drought-tolerant genes specific to pigeonpea. The
pigeonpea genome sequence reported one hundred eleven
(111) homologous sequences corresponding to universal
drought-responsive protein sequences from the Viridiplantae
( ). Transcriptome assembly (
), identification of genes for abiotic stresses tolerance of
pigeonpea were reported (
).The present
investigation involves identification, sequencing and
characterization of proteins with in-silico protein structure
prediction and domain analyses responsible for stress
tolerance and high yielding traits.
MATERIALS AND METHODS
Plant material
Through detailed evaluation and multi-location trials of cross
derivatives, we identified 65 better performing pigeonpea
lines. Among these lines, high yielding and stress-tolerant
accessions were identified.
Drought stress treatment and tissue harvesting
Seeds were treated with surface sterilants and then washed
with double distilled water, sown in pots filled with pot
mixture with soil collected from field and vermicompost.
Plants were grown under controlled conditions. For imposing
drought stress, slow drought stress was imposed on plants
when they reached 22 days old seedling stage. An exact
calculated quantity of water was added to each pot and
weighed at regular intervals. Control plants were maintained
at 80% relative water content (RWC) throughout whereas,
stressed plant growing pots were dried down gradually to
20% RWC. The transpiration ratio (TR)was recorded on a
daily basis to calculate the intensity of the drought stress.
Stressed plants weredriedthrough transpiration until the TR
reached 0.1. Tissues were harvested from the stressed plants.
Samples were slightlysmeared using 70% ethanol to remove
soil particles. All tissues were immediately frozen in liquid
nitrogen and stored at −80°C for RNA isolation.
RNA was isolated from pigeonpea leaves using TRIzol
Reagent (Sigma). Quality of sample was checked by agarose
denaturing gel (1.2%) and Nanodrop spectrophotometer.
nd
First-strand cDNA synthesis is done by Proto script 2 first-
strand c DNA synthesis kit (New England Biolabs) following
manufacturers instruction; second strand synthesis and PCR
amplification were performed in 20μl reaction mixture using
2ul first-strand cDNA mix. Each reaction mixture contained 2
μL of 10× PCR buffer A, 1.6 μLdNTPs (25 mmol/L), 2 μL
anchored oligo and arbitrary primers and 0.2 μL of 4U
TaqDNA polymerase. PCR reactions were performed using a
thermal cycler (G8800ASureCycler 8800 (M/S Agilent)
programmed to initial denaturation at 95ºC for 5 min,
denaturation at 94 ºC for 30 s followed by annealing at 62 ºC
for the 30s, extension at 72 ºC for 1 min for 40 cycles and then
followed by final extension at 72 ºC for 5 min.
Cloning and sequence analysis
After completing the amplification process products of
lanC–like GCL-2 protein, bop and btb/pozamplicons were parted
in 1.2 percentagarose gel. Single bands of each gene were
Varshney et al., 2012 Kudapa et al.,
2012
Sekhar et al., 2010;Priyanka et al.,
2010; Saxenaet al., 2011; Deeplanaik et al., 2013
Preparation of genomic RNA
expurgated from the gel, eluted and cloned in PCR4-TOPO
Vector (Invitrogen) for sequencing. Cloned sequences were
blasted with the NCBI BLASTN tool (http://blast.ncbi.nlm.
nih.gov) and aligned with earlier reported sequence using
CLUSTALW software. Putative encoding region of transit
peptides and mature proteins from different plant genomes
were predicted using Blast2go (https://www.blast2go.com).
Domain Prediction of lanc-like protein GCL2 and BOP gene
in Cajanus
Domain prediction for lanc-like protein GCL-2, BOP gene and
B T B / P O Z g e n e s h a s b e e n d o n e b y N C B I
(https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi) CD-
search software. Fasta sequence of BOP gene was retrieved
from NCBI (https://www.ncbi.nlm.nih.gov/nucleotide).This
blast search explained the diversity in the domain of BOP gene
family.
Protein Structure Prediction
Rapto rX s tr uctur e pre di ctio n soft wa re wasus ed
(http://raptorx.uchicago.edu/) to predict the protein structure.
RaptorX gives the appropriate results for the one or multiple
distantly related template proteins (especially those with
sparse sequence profiles) and quality of the alignment
between a target sequence and by a probabilistic-consistency
algorithm and a novel nonlinear scoring function. The results
obtained were downloaded in graphical form and as their
atomic co-ordinate files as well. PROCHECK was used to
validate the structure of predicted proteins.
Semi-quantitative PCR
RNA isolation has been done from pigeonpea lines developed
by our team with control (Asha, DGRg 55, DGRg 53, DGRg 56
and DGRg 58) plant leaves using TRIzol Reagent (Sigma).
Quality of RNA samples was checked by agarose denaturing
gel (1.2%) and Nanodrop spectrophotometer.
Primer 3 online tool was used to design specific primer for
qPCR amplification. Semi qPCR amplification was carried out
with KAPA SYBR FAST Universal qPCR Reaction Mix (qPCR
Reaction Mix from M/S KAPA BIOSYSTEMS), 1µl cDNA, 12.5
µl Reaction mix and 0.5M of each forward and reverse
primers. The volume used for it was made to 25l with
nuclease-free water. PCR tubes containing the above
components were capped and given a pulse spin to allow
proper mixing of the reaction mixture. PCR was carried out in
G8800ASureCycler 8800 (M/S Agilent) thermal cycler.
Gel electrophoresis
After completion of qPCR amplification, Samples were
loaded in 3.5% metaphor agarose gel and electrophoresed at
90V for 45 min in HE Plus (Hoefer). The gels were stained with
ethidium bromide. The resolved amplification products were
visualized by illumination under UV light in a gel
documentation system (Syngene).
RESULTS AND DISCUSSION
From our earlier MYB network and flowering genes
networks, we could identify tightly linked and co-expression
of genes for these traits. ( ).
First-strand cDNA synthesis and semi qPCR amplification
Dubos et al., 2010; Singh et al., 2017

[Journal of AgriSearch, Vol.6, No.3]
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Yasin et al
September, 2019
Semi-quantitative expression analyses showed that the
defensin type drought stress tolerance contributing lanc like
protein GCL-2 is expressed in providing disease resistance
and myb linked BTB/POZ genes contribute for high yielding
of pigeonpea ( ). BOP is a member of BTB
group of plant protein. We found these genes to get expressed
together in drought-tolerant high yielding pigeonpea lines
earlier reported by our team ( ) whereas in
Taddese et al., 2014
Couzigou et al., 2016
another report we explained the myb linked expression of
BTB/POZ genes. These genes selected from our earlier
network analyses were identified, PCR amplified and
sequenced. From the gene sequence, we have predicted the
protein structure and validated it. Lan C was found to be
associated with our co-expression analyses. This confirms
that these genes are directly contributing to stress tolerance
and high yielding traits.
Fig. 1: Domain details of BOP and BTB/POZ proteins
BTB/POZ and TAZ domain-containing protein may act as a
substrate-specific adapter of an E3 ubiquitin-protein ligase
com pl ex ( CUL3- RBX 1- BTB) whi ch med iat es the
ubiquitination and subsequent proteasomal degradation of
target proteins ( ). BTB/POZ and TAZ domain-
containing proteins (Fig. 1) family are essential for female and
male gametophyte development and hence contributing for
higher seed yield and seed weight. It acts redundantly with
BOP2 ( ). BOP1/2 promote leaf and floral
meristem fate and determinacy in a pathway targeting AP1
and AGL24. This mode of action leads to conversion of
vegetative to flowering phase, developing more flowers per
panicle and higher yield per plant. BOP1/2 act as
transcriptional co-regulators through direct interaction with
Boyle et al., 2009
Ha et al., 2004
TGA factors, including PAN, a direct regulator of AP1.
Controls lateral organ fate through.
BTB/POZ and TAZ domain proteins are Small Ubiquitin-like
Modifier (SUMO) ligase act as a substrate specific adapter of
an E3 ubiquit in ligase, express ionally related to the SUMO-
conjugating enzyme SCE1 (https://www.uniprot.org) and
guides the attachment of the small protein SUMO by
postranslational modification to target proteins via covalently
attached isopeptide bond ( ). It has
high similarity to the yeast UBC9 SUMO ligase (
). This enzyme exhibited higher sensitivity to ABA in root
growth inhibition assays.
Withers and Dong, 2016
Xu et al.,
2016
Fig. 2: LAN C protein domain details of C. cajan
Fig. 3: Predicted structure of LanC like GCL-2 Protein
C. cajan Lan C like GCL-2 protein ( ) sequence was
submitted to Raptor x Software. Raptor X predicts the
secondary and tertiary structure, solvents accessibility,
contacts, binding sites and disordered regions of the given
Fig. 2 and 3 input sequence. It is also assigned the confidence scores to
determine the quality of the structure. The predicted structure
was validated and presented ( ).Fig. 4

[Journal of AgriSearch, Vol.6, No.3]
Role of LanC in Stress and Yield trait of Pigeonpea
108
Gene expression analyses
Gene expression analyses were carried out for all selected
genes with four selected advanced breeding lines of
pigeonpea with control and housekeeping genes (either α-
Tubulin or β-Tubulin). Semi-Quantitative results indicating
over expression of these genes in selected lines were depicted
in . For Ccbt we could find two variants of
the gene.
figures 5, 6, 7 and 8
Fig. 4: Ramachandran plot for LANC protein structure validation
Fig. 5: Ccbtb gene expression (Ladder Marker: 100 bp DNA Ladder,
Lane A1: Asha, Lane B1: DGRg 55,Lane C1 :DGRg 53,Lane D1: DGRg
56, Lane E1: DGRg 58 and Lane T: α-Tubulin).
Fig. 6: Ccbt (Ladder Marker: 100 bp DNA Ladder, Lane A13: Asha,
Lane B13: DGRg 55, Lane C13 :DGRg 53,Lane D13: DGRg 56, Lane
E13: DGRg 58 and Lane T1: α-Tubulin)
Fig.7: Ccbop1(Ladder Marker :100bp DNA Ladder , Lane A1: Asha,
Lane B1: DGRg 55, Lane C1 : DGRg 53,Lane D1: DGRg 56, Lane E1:
DGRg 58 and Lane T: β-Tubulin)
Fig.8: Comparative up and down regulation of genes in different
lines of pigeonpea
Gene Network
Predicted gene coexpression network is present in . This
co-expression of genes confirms our earlier reports and
depicts the network of the gene required by high yielding
plants.
BOP Gene
BLADE-ON-PETIOLE 1 (BOP1) and BOP2 encodinggenes
are redundant transcription factors restricted to the base of
developing lateral organs including the leaf and floral
development (
).
The BOP genes encode proteins containing a BTB/POX VIRUS
AND ZINC FINGER (POZ) domain and ankyrin repeat(
Fig. 9
Ha et al., 2004; Norberg et al., 2005; Hepworth et
al., 2005
Ha et

[Journal of AgriSearch, Vol.6, No.3]
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Yasin et al
September, 2019
Fig.9: Network of genes directly correlated with yield and drought tolerance traits

[Journal of AgriSearch, Vol.6, No.3]
Role of LanC in Stress and Yield trait of Pigeonpea
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).
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).
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). However,
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)
CONCLUSION
The predicted networks of genes were found to be the best for
further research. Identified genes and their expression
analyses suggest that they could be the best candidates for
screening germplasm for variations in identifying donor for
crop improvement research.
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