INTRODUCTION
Maize (Zea mays L.), belonging to family Poaceae is the major grain and fodder
crop worldwide. It is also known as the "Queen of Cereals'' since it has the
highest genetic potential and is a C4 plant, originated in Central America and
initially domesticated in Mexico, before being transported to India (Kumar et al
2012). It is the third most important food crop in India after rice and wheat.
Maize is grown on 183 million hectares of land worldwide, with a total production
of over 717 million tonnes and an average productivity of about 5.0 tonnes per
hectare. In India, it is grown on 9.38 million hectares, with a maximum
production of 28.75 million tonnes and an average productivity of about 3.07
tonnes per hectare (Reddy et al 2019). Majority area in India i.e. about 78 per
cent is sown during kharif season, while the remaining 20 and 2 per cent falls in
rabi and summer season, respectively (Yathish et al 2019). Andhra Pradesh,
Karnataka, Rajasthan, Maharashtra and Bihar are the states where it is
distributed most widely. In addition to being the ideal cereal fodder crop
throughout the summer, early winter and rainy seasons, maize is an important
grain crop during the kharif season. In Punjab, grain maize was cultivated in
107.8 thousand hectares during 2020-21, with a total production of 395.1
thousand tonnes. In contrast, the fodder maize cultivation area in Punjab was
0.78 lakh hectares (Anonymous 2022). Fifteen per cent of the total protein and
nineteen per cent of the total calories are present in maize grains (Reddy et al
2019). Maize is used for many purposes, including human consumption (24%),
poultry feed (52%), animal feed (11%), raw materials for many different
industries (11%), seed (1%) and brewing (1%) (Reddy et al 2019).
The genetic diversity of the maize crop makes it a potential source of genes for
essential agronomic traits including adaptation to local growing conditions
through selection under artificial pressures created by farmers (Berg 2009) and
tolerance to biotic and abiotic conditions occurs naturally (Mahar et al 2009). A
number of biotic stresses especially insect infestation, hinder the production of
maize. Insect pests can attack every part of the plant, at any stage of crop
growth, from the high valleys of the tropics and subtropics to the tropical
lowlands and temperate zones (Ortega 1987). About 250 different insect and
mite species have been identified in the maize crop, with the spotted stem borer
Chilo partellus (Swinhoe), shoot fly Atherigona spp. (Rondani) and pink stem
borer Sesamia inferens (Walker) being the most widespread pests and in some
cases, causing yield losses of up to 80 per cent (Reddy 2001). Fall armyworm,
Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), a harmful
polyphagous, invasive, highly mobile and destructive pest was found in maize for
the first time in North and South America in 2016, in Argentina and the
Caribbean region (Ghimire and Bhetwal 2021). In the majority of North America,
it sporadically spreads and then eventually dies during the harsh winter months,
but in the majority of Africa, fall armyworm generations are continuous all year
long wherever host plants are present, including off-season and irrigated crops,
when climatic conditions are favourable (Prasanna et al 2018a). In May 2018, the
Shivamogga district of Karnataka (India) received the first case of the fall
armyworm pest from Asia (Sharanabasappa et al 2018a). The fall armyworm
spreads quickly thereafter in the entire country due to its high rate of
transmission (Suby et al 2020). The ICAR-IIMR recently identified the pest in
Punjab on grain maize (Rakshit et al 2019). In August 2019, fall armyworm
infestation was also observed in fodder maize fields in Hoshiarpur (Cheema et al
2021).
The name "fall armyworm" refers to their mode of attack, which involves
infestation spreading over wide agricultural fields and consuming every plant
matter, they come across in their broad dispersals, giving them the impression of
a massive army (Smith 1797). Despite the fact that fall armyworm has been
shown to consume more than 350 plant species (Montezano et al 2018), its
preference for the Gramineae family has led to it being referred to as a "pest of
grains." By October 2021, 76 countries (47 in Africa, 23 in Asia and 6 in Oceania)
had been infested by the fall armyworm outside of its normal habitat (CABI
2021). It has multiple generations per year and may travel up to 100 kilometres
in a single night. The most significant variables influencing the growth and
spread of fall armyworm (Wang et al 2020) and their natural enemies are
temperature and precipitation in addition to host availability (Lopez et al 2018,
Montezano et al 2018). A proper and effective management strategy requires
proper pest identification. Fall armyworm affects maize plants at every stage of
growth, from seedling to tassel, with its primary targets being crop growth
points, young leaves, leaf whorls, tassels and cobs. It mostly results in
defoliation, scraped leaves, pinhole and windowpane symptoms, young plant
mortality, grain loss, decreased yield quantity and quality (FAO 2018). During the
crop's vegetative stages, the pest causes leaf skeletonization and windowed
whorl (Shylesha et al 2018). According to FAO (2020), due to the fall armyworm's
rapid expansion and potential for crop destruction, food insecurity and rural
poverty may rise.
Fall armyworm effect can be reduced by using integrated pest management
techniques, chemical control, genetic resistance, cultural practices, mechanical
control and local control. Excessive pesticide usage for pest management is not
permissible since maize is directly ingested as feed by cattle. Additionally, in
some regions of the world, S. frugiperda has already evolved resistance to the
majority of pesticides (pyrethroids, organophosphates and carbamates) (Mota-
Sanchez and Wise 2017). Its management hence requires inclusion of cultural
practices such as changing planting dates, crop rotation, burning crop residues
and removing alternate hosts near to maize fields in the management
programme, which though may not be successful in smallholder agricultural
systems (Kumar et al 2022). Natural enemies such as parasitoids,
entomopathogenic fungi and nucleopolyhedroviruses have also been found
associated with the pest (FAO 2018), smallholder farms, these natural enemies
are, however, either challenging to come across or are only available
commercially. Genetically modified (GM) maize cultivars that express Bacillus
thuringiensis (Bt) toxins can also be used to control the pest.
The goal of the host plant resistance (HPR) management is to identify and exploit
germplasm that naturally resists the fall armyworm. Since it is an affordable,
biological, socially acceptable and environment friendly alternative to pesticides,
it is a promising technique and an essential part of any pest management
approach, also suitable for fall armyworm too (Prasanna et al 2022). The
potential to reduce feeding damage from insect pests can be through different
mechanisms like antixenosis, antibiosis and tolerance (Painter 1951).
"Antixenosis" refers to the presence of morphological or chemical components in
a plant that change insect behaviour, reducing pest’s ability to establish as
reflected by poor feeding, rejection of oviposition and delayed acceptance as
host. The biological impact of the host plant on insect is known as "Antibiosis"
leading to low survival rate, longer development period and low adult fecundity
due to biochemical factors (Smith 2005). The ability of a plant to resist an insect
pest attack and still produce its best yield with minimal yield loss is referred to
as tolerance. For integrated pest management to be successful, it is important to
use resistant or moderately resistant plants, as they may help to reduce pest
populations to a level that does not harm the environment, upset the ecosystem
or result in grower losses (Smith 2005). Without increasing expenses, pest
management is assured in resistant cultivars along with the seed. In a
programme to breed resistant cultivars with other desirable features, a wide
range of germplasm is tested for its reaction to pests and the best germplasm is
employed in target-specific breeding programmes. Mass rearing insect in large
number and evaluating the germplasm under artificial infestation is a part of
such programmes.
Since 1980s, the International Maize and Wheat Improvement Center (CIMMYT)
have been working to establish germplasm that is resistant to insects. Multiple
borer-resistant (MBR) and multiple insect-resistant tropical (MIRT) inbred lines
and populations have been developed. Several researchers have examined how
inbred maize lines interact with fall armyworm larvae (Brooks et al 2005, Ni et al
2008 and Paul and Deole 2020a). Using germplasm with a similar genetic
structure, antibiosis and non-preference were discovered to be the resistance
mechanisms against fall armyworm. Moreover, there are biochemical differences
between the susceptible and resistant maize genotypes (Williams et al 1989). It
is necessary to investigate various genetic resources and find promising maize
genotypes for fall armyworm resistance breeding (Prasanna et al 2018a).
Evaluating a variety of maize germplasm, including landraces, improved
varieties, open pollinated varieties and synthetic varieties could help to identify
parental germplasm with a broad genetic potential for fall armyworm resistance
(Kasoma et al 2020). In order to use them as sources of resistance in plant
breeding programs or to help farmers choose the most promising cultivars for
pest management, it is essential to identify maize landraces that are resistant to
insect pests. days.
To overcome insect herbivory, plants have evolved well defined phenolic
pathways and defensive mechanisms that aim at evading pest attack by
producing compounds that modulate defence mechanisms(Pannutiet al
2015).Phenolic compounds are biologically active secondary metabolites that
play a fundamental role in determining tolerance of plants towards biotic
stresses (Pannuti et al 2015).The release of secondary phenolic metabolites
from host plant can affect insect oviposition rate, lowers the larval growth
and decrease the pupal mass(Collison et al 2015).Plants also show resistance
to insect feeding with cell wall modification such as accumulation of cell wall-
bound phenolics, association of defensive proteins such as lignins, suberin and
cuticle-associated phenolics(Pannuti et al 2015). These compounds may act as
feeding deterrant and prevent arthropod feeding (Burtet et al 2017).
Extensive transcriptome reprogramming that activates the expression of
phenolics and defensive proteins such as protease inhibitors, release of
secondary signal transduction components, activation of pathogenesis-related
genes along with defense related transcription factors in response to fall
armyworm infestation has been reported to inhibit larval growth and
development thus reducing tissue damage (Zhou et al 2020 ;Dafoe et al
2013).The biosynthesis of phenolic compounds occur through shikimate
pathway, which involve the participation of two major amino acids
phenylalanine and tyrosine along with enzymes of shikimate pathway
including phenylalanine ammonia lyase, tyrosine ammonia lyase,
polyphenol oxidase, peroxidase etc. The level of complexity ranges from
simple phenolic molecules such as phenolic acids(coumaric acid, cinnamic
acid) to highly polymerized compounds such as lignin and tannins. Lignin is a
phenolic heteropolymer that limits the insect feeding by increasing the leaf
toughness and lowering the nutritional content of the leaf (Johnson et al
2017).Quinones formed by polyphenol oxidase (PPO) and peroxidase (POD)
catalyzed oxidation of phenols bind covalently to leaf proteins and inhibit
the protein digestion in pest (Bhonwang et al 2015).The core strategy used by
plants to counter the pest attack is based on the process of biosynthesis,
release and finally accumulation of phenolics and defensive proteins (Boller and
He 2009;Lu 2009). Flavonoids are cytotoxic and interact with different
enzymes through complexation. It includes flavonols, anthocyanins and
proanthocyanidins.Overexpression of flavonoid producing transcription factor in
Arabidopsis had been reported to provide resistance against Spodoptera
frugiperda. It protects thehost plant by inhibiting feeding, oviposition and
population build up of pest (Xu et al 2019). Insect-plant interaction results in
the formation of defensive proteins including lectins, phytoanticipins,
phytoalexins (such as hydroxycoumarins and hydroxycinnamate conjugates)
and enzymes like glucanase, chitinase, proteaseinhibitors (Akhtar and Malik
2000;Lattanzioet al 2006).Protease inhibitors bind and inhibit the activity of
digestive enzymes inside insect gut thereby lowering protein digestion, causing
shortage of amino acids and leading to starvation of the insects. Since, maize
(Zea maysL.) has been reported to be adversely affected by fall armyworm
infestation (Boudron et al2019), we planned to study the phenolic metabolism
and defensive status of maize during fall armyworm infestation. Maize has
a wide economic importance with global production of 1148million tons (FAO
2020). In India, it occupies9.9million hectares and contributes to a production of
30 million tonnes (USDA 2021). The name―miracle crop‖ is given to maize due
to its wide adaptability and diverse uses as food, feed and biofuel production
(Cassidy et al 2013).On the basis of genetic evidence teosintes has been
proposed to be direct ancestors of maize(Beadle1980). Extensive
microsatellite genotyping based studies confirmed Balsas teosinteas the
progenitor of maize (Matsuoka et al 2002).In teosinte, plant architecture is
remarkably described by teosinte branched1 - domestication gene‘. The
modification in teosinte glume architecture1gene leads to removal of protective
casing around teosinte and give rise to maize grains that were readily
consumable (Dorweiler et al 1993).
It has been reported in literature that the wild genotypes show high tolerance
against biotic stresses as compared to the cultivated plants. Therefore, we
planned to explore the phenolic and defensive status of the wild progenitor
of maize, teosinte, that might help in decephering the tolerance mechanisms
adapted by plants against pest infestation.
The current research aimed to see how fall armyworm responds to various maize
inbred lines under Punjab conditions, so the objectives of the study were:
