Abstract
Main conclusion
Understanding surface defenses, a relatively unexplored area in rice can provide valuable insight into constitutive and induced defenses against herbivores.
Abstract
Plants have evolved a multi-layered defense system against the wide range of pests that constantly attack them. Physical defenses comprised of trichomes, wax, silica, callose, and lignin, and are considered as the first line of defense against herbivory that can directly affect herbivores by restricting or deterring them. Most studies on physical defenses against insect herbivores have been focused on dicots compared to monocots, although monocots include one of the most important crops, rice, which half of the global population is dependent on as their staple food. In rice, Silica is an important element stimulating plant growth, although Silica has also been found to impart resistance against herbivores. However, other physical defenses in rice including wax, trichomes, callose, and lignin are less explored. A detailed exploration of the morphological structures and functional consequences of physical defense structures in rice can assist in incorporating these resistance traits in plant breeding and genetic improvement programs, and thereby potentially reduce the use of chemicals in the field. This mini review addresses these points with a closer look at current literature and prospects on rice physical defenses.
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Introduction
Rice, Oryza sativa L. (Family: Gramineae) is the major staple food crop cultivated and consumed by more than half of the global population (Sharif et al. 2014). Rice is the third most important crop after sugarcane and maize, in terms of production and is cultivated in more than 100 countries with an annual production of nearly 510 million tons of milled rice across 165 million hectares, with significant contributions from China, India, Indonesia, Bangladesh, and Vietnam. Major rice exporters include India, Thailand, Vietnam, and Pakistan, and are mainly imported to the Sub-Saharan Africa region accounting for 31% of the overall global imports (USDA 2022). According to FAO (2018), the five major importers of rice are China, Nigeria, the Islamic Republic of Iran, Saudi Arabia, and the Philippines—expected to be one-third of the global rice imports by 2027. Clearly, rice production is critical for food security on planet Earth. However, like most cultivated crops, rice also suffers from multiple stressors under different production systems across the world.
Stress in plants can be defined as the external conditions that negatively impact a plant's growth, development, or yield (Verma et al. 2014) and can be categorized as abiotic or biotic stress. Abiotic stress is caused by the environment and can be either physical or chemical, whereas biotic stress is caused by living organisms, such as viruses, bacteria, fungi, nematodes, insects (Table 1), and weeds. To avoid the selective pressure imposed by these stresses, plants have developed incredible defense mechanisms. Plant defenses can be either direct or indirect (Karban and Baldwin 1997; Howe and Jander 2008). Direct defenses are types of defenses that exhibit a pernicious effect on herbivores affecting their mobility, feeding, growth, and development (Kessler and Baldwin 2001). On the other hand, indirect defense is the attraction of natural enemies toward the plants by the volatiles released during the attack i.e., herbivore-induced plant volatiles (HIPV) (Kessler and Baldwin 2002; Arimura et al. 2005; Howe and Jander 2008Kariyat et al. 2012) or through extra floral nectaries (Rosumek et al.2009; Heil 2015) that is found to be increased/ induced by insect herbivory and initiate more parasitism and predation (Jones et al. 2017). Although plant defenses and insect counter defenses have been meticulously examined, most of these studies have ignored the first line of defense—plant surface defenses and focused more on the chemical defenses (Qi et al. 2018; Lu et al. 2018; Shi et al. 2019; Kariyat et al. 2017). In dicots, extensive research has been conducted to understand their defense systems against herbivorous attacks, particularly in model plants such as Arabidopsis (Arabidopsis thaliana (L.) Heynh.) and tomato (Lycopersicon esculentum (Mill.) (Wu and Baldwin 2010; Stam et al. 2013; Wang and Wu 2013), and in a wide range of wild and domesticated, model, and non-model species (Philipe and Bohlmann 2007; Xing et al. 2017; Feng et al. 2021; Johnson et al. 2021; Lefebvre et al. 2022; Kaur and Kariyat 2023). However, monocots, an important group that includes most of the staple food crops including rice, have been less studied, in physical and structural defenses. Here, we review and summarize the previous studies on physical defenses, their mode of action, and then specifically evaluate these defenses in rice, and suggest potential areas for future research.
Physical defenses and their role against insect herbivores
Physical or structural barriers, which are often regarded as the first line of protection against herbivory, are direct defenses that include cuticle, wax, spines, trichomes, and thickening or lignification of the cell wall. These are structural modifications in plants that negatively impact herbivores and work in a distinct way to contribute to the integrated defense phenotype of plants. Interestingly, most of these defenses have been evolved against abiotic stressors, later diversified to be a major defense against biotic stressors (Kaur and Kariyat 2020). Among the structural barriers, the cuticle is the outermost layer composed of lipophilic compounds, laid over the epidermis protecting the plants from both biotic and abiotic stresses (Hanley et al. 2007; Agrawal et al. 2009). One of the most vital components of the cuticle is wax, the outermost protective barrier, and those dispersed on the surface of lipophilic polymer are called epicuticular wax (EW) (Wójcicka 2015). Wax can alter the feeding, movement, and foraging behavior of insect pests, predators, and parasitoids (Eigenbrode 2004), and the effects are species specific. For instance, in crucifers, the presence of long-chain alcohols and amyrins in the leaves reduced the infestation of the destructive diamondback moth, Plutella xylostella L. (Eigenbrode and Pillai 1998). Similarly, Watts and Kariyat (2022) studied the effects of epicuticular wax on tobacco hornworm, Manduca sexta by comparing two different species of Solanum (Solanum glaucescens Zuccarini and Solanum macrocarpon Linnaeus), the former with the highest wax and least trichomes, and latter with no wax and highest trichome density. They found epicuticular wax in S. glaucescens can act as a powerful barrier against M. sexta leading to the reduction in mass gain and increased mortality even when the species has the least trichomes. However, the role varies depending on the pests as in pea, Pisum sativum L., where fewer wax blossoms resulted in a reduction in aphid infestation but more severe weevil damage. (White and Eigenbrode 2000). Spines are another surface defense structure that are sharp, needle-like modifications of petioles, midrib, or spicules that disrupt the feeding, mobility, dispersal, and mating behavior of herbivores (Hanley et al. 2007; Portman et al. 2015; Kariyat et al. 2017). In Solanaceae, Manduca sexta preferred to defoliate plants with fewer spines, and opted quickly for leaves with no spines that are removed for the experiments compared to leaves with intact spines, confirming the role of spines in defense (Kariyat et al. 2017). Similarly in 2023, Johnson et al. investigated the effects of epicuticular wax of, Aloe barbadensis against M. sexta and S. frugiperda and found the surface waxes and volatiles emitted from the wax when added on artificial diet prevented them from feeding, also concluding the effects of wax affecting the growth and development of insect herbivores.
When compared to other surface barriers, trichomes are important, have undergone extensive research, and play a vital role in plant–biotic interactions (Kariyat et al. 2013, 2017). Trichomes are unicellular or multicellular hair-like appendages that advance outward (Werker 2000). They originate from the epidermal cells of vegetative and reproductive plant structures (Oksanen 2018) and have a negative impact on herbivores by preventing or impeding their movement or by delivering toxins that affect their growth and development (Agren and Schemske 1993; Kaur and Kariyat 2020). In addition to protecting against herbivores, they also provide defense against abiotic stresses such as UV radiation, water loss, and extreme temperatures (Ehleringer 1982; Li et al. 2018; Oksanen 2018). They can be divided broadly into glandular and non-glandular types (Werker 2000). Non-glandular trichomes are unicellular, tough, and sharp, blocking the entry or causing physical injury to insects (Dalin et al. 2008) and vary in their density, length, and orientation in different plant species (Cho et al. 2017; Kariyat et al. 2017, 2019; Watts and Kariyat 2021) whereas glandular trichomes are multicellular structures that trigger the genes that protect against insect herbivores by releasing toxic substances (Peiffer et al. 2009).
Lignification or cell wall thickening is another defense mechanism plants adopt in response to herbivory. Lignin is one of the most important phenolic acids and is the second most abundant polymer after cellulose, synthesized by phenylpropanoid pathway. Lignin is present in the cell wall of plants, imparting resistance to biotic and abiotic stresses in addition to structural support. Lignin is responsible for the toughness of tissue that can resist herbivore damage (Raupp 1985), -the tougher the tissue, the more the lignin is. In maize, lignin reduced the palatability to chewing insects by regulating the lignification process (Santiago et al. 2013) and by the effect of phenoloxidase enzymes that are involved in the lignin biosynthesis process. Phenoloxidase enzymes has also an important role in the production of toxic byproducts such as reactive oxygen species, peroxides, and quinones that are detrimental to herbivores (Felton et al. 1989; Gandhi et al. 2021). In general, the physical defenses in the plants have a great potential to tolerate herbivory and unveiling the role of each defense in depth can be used to modify and breed plants by regulating host plant resistance to reduce the attack from insect pests.
Physical defenses in rice
Epicuticular wax
In rice, epicuticular wax (EW) has been found to play an important role in the defense against herbivores. Brown plant hopper (BPH), Nilaparvata lugens (Stal), a major sucking pest, has been found to alter its preference for the host by the presence of hydrocarbons and carbonyl groups in the wax. Woodhead and Pudgham (1988) investigated the non-preference of BPH on to the stem of variety IR46 compared to other varieties and their tendency to move from stem to the leaves of the variety, even though they prefer stems, thus concluding the role of wax as a structural barrier. The importance of EWs in the reduction of infestations of two important pests of rice, rice water weevil, Lissorhoptrus oryzophilus (Kushal), and fall armyworm, Spodoptera frugiperda (J.E. Smith) was explored using mutants with reduced epicuticular wax in comparison with wild-type plants. When the female weevils were given a choice for oviposition, the number of larvae emerging from the mutants was higher than the ones that emerged from a wild type that has the normal wax amount. In addition, the weight gained by the fall army worm larvae were found to be higher in mutants compared to wild-type plants confirming the role of wax in defense against herbivores (Bernaola et al. 2021).
Shi et al. (2023) recently showed that there are 19 wax compounds in rice leaves and sheaths that include acids, alkanes, aldehydes, and alcohols such as hexacosanoic acid, triacontanal, octacosanal, pentacosane, 1-tetracosanol to name a few. In addition, they also found a strong relationship between soil nitrogen and the age of rice plants, with the wax composition and content. Researchers concluded that as the plants age, wax content increases and can thereby suppress pest attacks as part of physical defense. In addition, nitrogen has an important role in determining the wax composition as the content of acid and alkanes in wax were found to increase under reduced nitrogen levels, suggesting the negative effect of nitrogen on wax content. However, more in-depth research will be required to ascertain what aspects of rice EWs may be influencing the behavior of herbivores, and more importantly, whether rice EW quality and quantity can be altered by herbivory, and herbivore feeding types. More recently, a study of sorghum against sugarcane aphids found that wax components such as α-amyrin and isoarborinone were found to increase in 10-day sorghum plants after aphid infestation (Cardona et al. 2023).
Trichomes
Trichomes in rice have been found to differ in terms of density, length, degree of hardness, growth direction, and form type (Xiao et al. 2017), and can also vary among varieties. In rice, it is commonly observed that the trichome density and their distribution are not uniform. However, a higher trichome density is found on leaves and glumes, compared to other plant parts. Among leaves, there are three different types of trichomes commonly observed—micro, macro, and glandular hairs. Macro hairs are observed in silica cells; whereas, micro and glandular hairs are found on stomatal cells or beside the motor cells (Li et al. 2010). Khetnon et al. (2022) showed that rice can have four types of non-glandular trichomes: prickle, macro, micro and papillae trichomes (Fig. 1). Characterizing its distribution over different varieties, Viz and Pacada (2022) investigated the trichome profiling of the traditional rice varieties and found variations among them and found a specific pattern in their density and dispersion and concluded, trichomes were densest (4.56–5.46/mm2) and mostly dispersed (49.09–50.53%) in the apical zone of the leaf surface, and least dense (2.62–2.83/mm2) and rarely distributed (16.44–18.81%) in the basal zone. This discovered pattern of diminishing trichome density and distribution on the adaxial leaf blade surface from the apical zone to the base zone can be potentially used for developing varieties that might help defense against rice stem borers through enhanced structural defenses. There is also variation in the orientation of trichomes, wherein they are either erect or recumbent (Viz and Pacada 2022) Considering the two types, more erect hairs can potentially act as a better barrier against pests like stem borers (yellow stem borer and white stem borer) to deter oviposition (as observed in other species (Levin 1973; Hawthorne et al. 1992; Juvik et al. 1994; Resende et al. 2006; Murungi et al. 2016), and thus, decrease infestation, although empirical evidence is currently lacking.
In Punithavalli et al. (2013) examined the function of rice trichomes against the rice leaf folder, C. medinalis, and demonstrated their significance in preventing larval migration and the challenge of the larvae for creating folds for feeding within. Sandhu and Sarao (2021) reported that the population of nymphs and adults of BPH were much lower in genotypes with longer and denser trichomes than in susceptible genotypes such as TN1. However, Khetnon et al. (2022) claimed that the physical defense by trichomes was not effective against BPH because trichomes were not tough enough to prevent colonization by the second and third instars. According to Karban et al. (2002), the removal of silicified non-glandular trichomes in rice increased the frequency of damage to leaf sections including the basal region, which was not preferred by the herbivores in the presence of unidirectional structures. Researchers concluded that unidirectional structures such as trichomes are involved in directing the herbivore movement and, hence, can be adopted in plant breeding programs against insect pests. In addition, Andama et al. (2020) demonstrated the vital role of trichomes in imparting defense against insect pests indiscriminately affecting both generalists as well as specialists. Nerica, a new interspecific hybrid rice variety used in Africa was found to be more infested when compared to the local Japanese variety, Nipponbare even when the former has a strong volatile profile. In connection with this, they found the presence of non-silicified glandular trichomes in Nipponbare compared to Nerica, and the larvae fed on Nipponbare showed a higher mortality rate. Larvae fed on Nipponbare on dissection were observed with prevalent punctures and holes in the midgut as well as found strong undigested trichomes from the frass stressing out the pivotal role of trichomes in defending the herbivory (Andama et al. 2020) as previously observed in other systems (Kariyat et al. 2017).
Callose deposition
Callose, a β-(1,3)-D-glucan polymer, plays an important role against phloem-feeding insects and pathogens in the plants by depositing callose at the site of the attack to slow down their feeding and spread (Miles 1999). Callose is usually present in sieve plates of phloem, pollen grains, pollen tubes, and pollen mother cells in plants (Stone and Clarke 1992). During feeding by phloem-feeding insects, plants up-regulate genes encoding callose synthase and β-(1,3)-D-glucanases, activating callose synthase genes that initiate the callose synthesis and deposition of callose on the sieve plates of plants (Will and van Bel 2006; Kempema et al. 2007; Louis et al. 2012; Mondal et al. 2018; Varsani et al. 2019). The callose deposited on the sieve plates obstructs the sieve tubes and prevents the insect's penetration and feeding. However, β-(1,3)-D-glucanase can degrade the callose permitting phloem feeders to continue feeding significantly more in susceptible plants compared to resistant plants resulting in heavy damage to the susceptible rice plants (Hao et al. 2008). Callose deposition is also induced by the stress hormone, Abscisic acid (ABA) where Liu (2017a), explained the exogenous application of ABA can reduce the activity of the hydrolyzing enzymes and thus callose synthesis is unaffected. Here, the ABA showed a positive impact on rice by increasing its resistance to BPH, reducing its fecundity, and eventually acting as a barrier against the piercing and sucking insect pests; however, the exact mechanism behind this remains unresolved.
Lignin
Lignin is present in the cell wall of plants and in rice, lignin content varies from 10 to 14% (Wijayanti et al. 2019) depending upon the varieties and has an important role in preventing herbivory. Lignin accumulation in cell wall helps in imparting resistance to BPH (Jannoey et al. 2015; Guo et al. 2018; He et al. 2020) and according to Zheng et al. (2020), in addition to the callose deposition in response to BPH attack, lignin helps in providing mechanical rigidity to the rice sheaths, making it difficult for them to penetrate their stylets. This was in line with the findings of Wijayanti et al. (2019) who reported that having higher lignin and cellulose content tends to resist BPH attack. According to Zhang et al. (2022), regulated genes related to BPH attack are engaged in the synthesis of lignin and flavonoids, which demonstrates the post herbivory induction of lignin and its function as a physical barrier against important sucking pests in rice. Although the majority of research on lignin production is related to sucking pests, there have been few studies on chewing insect pests in rice, such as leaf rollers. Tianpei et al. (2015) showed that treating rice with an insect-specific peptide LqhIT2 was found to increase the accumulation of lignin resulting in imparting resistance to leaf roller. In addition, fertilization also has a strong impact on the lignin accumulation in rice, especially nitrogen fertilizers. A study conducted by Zheng et al. (2021), reported that low nitrate content (with a concentration of 0.3 mM KNO3) can increase the lignin concentration as well as other defense compounds such as flavonoids, phenolic acids, and saccharides, which have also been implicated in imparting resistance against insect pests—especially flavonoids (Kariyat et al. 2019; Tayal et al. 2020; Singh et al. 2021). Clearly, lignin helps in acting as a passive barrier as well as initiating other defenses in plants, in this case, against the striped stem borer, C. suppressalis. Collectively, these studies show the importance of lignin as an important component of physical defenses in rice.
Silicon
Silicon (Si) is the most abundant element in the earth's crust and has a crucial role in providing resistance against insect pests including chewing (florivores and borers) and sucking herbivores (phloem and xylem feeders). Si has direct effects on reducing the herbivore performance and indirect effects on the attraction of natural enemies by delaying the overall herbivore establishment (Reynolds et al. 2009). There are different forms of silica cells, such as butterfly-shaped in rice and maize, and oval-shaped in wheat (Alhousari and Greger 2018), and their cell differentiation is mediated by the phytohormone, jasmonic acid (JA). Si increases plant resistance by depositing silica, especially in opaline phytoliths. Phytoliths are the minute amorphous silica structures that are formed by the precipitation and polymerization of silica within and between plant cells (Piperno 2006). This helps in increasing the hardness and abrasiveness of plant tissues followed by reducing the digestibility (Kaufman et al. 1985; Salim and Saxena 1992; Panda and Khush 1995; Ma et al. 2001; Massey et al. 2006; Massey and Hartley2008), and causing mandibular wear in herbivores (Djamin and Pathak 1967; Dravé and Laugé 1978; Ramachandran and Khan 1991) and the degree of wear has a positive relation with the silicon concentration (Massey and Hartley 2008). Molting of mandibles occurs in each instar and, hence, mandibular wear cannot be only considered for the negative impacts in herbivores; moreover, destructive effects on silica on the digestive tract will add the impact as the digestive tract never molts reducing the nitrogen absorption leading to drastic reduction in the relative growth rate (Massey and Hartley 2008) and survival rate of caterpillars (Han et al. 2016).
Rice can normally absorb 300–700 kg/ha Si (Snyder et al. 1986) during different growth stages and hence has an important role in imparting resistance against herbivory (Mitani et al. 2005) (Table 2). The genetic evidence of the role of Si in imparting resistance was proved by Nakata et al. (2008), where the damage by the lepidopteran pests, rice leaf folder, C. medinalis, and rice green caterpillar, Naranga aenescens was more pronounced in Si-impaired low silicon rice 1 (lsil) mutant than the wild-type plants. Quite a few studies have demonstrated the role of Si in reducing the infestation of chewing herbivores of rice: rice stem borer Chilo suppressalis (Sasamoto 1958; Djamin and Pathak 1967; Drav´e and Laug´e 1978) and leaf folder larvae, C. medinalis (Hanifa et al. 1974; Ramachandran and Khan 1991). Studies have also shown that the presence of Si can increase the penetration time of insects to plants as in Asiatic rice borer, C.suppressalis (Hou and Han 2010). Subbarao and Perraju (1976) reported a significant reduction in insect infestation along with increased Si plant uptake with the soil drench of potassium silicate (K2SiO3) in rice against S. incertulas. In addition, Si can trigger the plants to produce, escalate or alter HIPVs (Herbivore Induced Plant Volatiles) that can either repel insect pests or attract natural enemies (Kvedaras et al. 2010). Liu et al. (2017b) reported a significant increase in the attraction of parasitoids, Trathala flavo-orbitalis and Microplitis sp. to Si-treated plants after the infestation of rice leaf folder. There was a variation in the HIPVs produced such as hexanal 2-ethyl, α-bergamotene, -β-sesquiophellandrene and cedrol, in infested Si-treated plants compared to non-treated plants, and the signaling pathway responsible for inducing resistance is JA. Similarly, Lu et al. (2015) reported the improved resistance of Si-treated plants against rice water weevil which is mediated by JA signaling. In short, Silica has a crucial role in rice in determining the degree of resistance toward defoliators.
In addition to defoliators, Silica also has a strong negative impact on piercing and sucking pests in rice. In phloem feeders such as BPH, Yang et al. (2017a) reported a significant decrease in the infestation in Si-treated rice. Here, Si deposition prolonged the time in the stylet pathway, thereby shortening the duration of phloem puncture and ingestion. Si deposition increased the hardiness and toughness of plant tissues, making BPH difficult to penetrate the tissues by the elongation of non-probing and stylet pathway activities. Another reason for this is the increased deposition of callose that obstructs the mass flow of the phloem, blocking the phloem sap leakage (Hao et al. 2008). Si also plays a role in the biochemical and physiological changes in plants by decelerating the increase in malondialdehyde (MDA) concentrations that attenuate the stress from BPH attack. In addition, Si can reduce the palatability of plant tissues through the activities of polyphenol oxidase and peroxidase phenylalanine ammonia lyase that catalyze the oxidation of phenols to quinones (Yang et al. 2017a). Hence, these studies conclusively demonstrate that silicate supplements can stimulate a variety of plant defense mechanisms against both chewing and phloem-feeding insect invaders by modifying plant secondary metabolites and antioxidant defense mechanisms.
Genes involved in surface defenses in rice
In rice, there are three important genes that are identified to be involved in trichome formation. GLABROUS RICE 1 (GLR1, otherwise known as WUSCHEL-LIKE HOMEOBOX 3B [OsWOX3B], DEGENERATIVE PALEA [DEP], and NUDA—a gene encoded by a WUSCHEL (WUS)-like homeodomain protein that assists in trichome formation. Another is HAIRY LEAF 6 (HL6) which interacts with OsWOX3B, encoding APETALA2/ETHYLENE RESPONSE FACTOR-type transcription factor initiating the trichome elongation and formation. SQUAMOSA PROMOTER BINDING PROTEIN-LIKE10 (OsSPL10), is the recently identified gene also found to be responsible for trichome production. Sun et al (2017), reported that HL6 interacts with OsWOX3B to form a protein complex that increases the binding of HL6 with an auxin-related gene, OsYUCCA5 leading to the development of trichomes. In a recent study, Li et al. (2021) confirmed the role of OsSPL10, by disrupting the gene by genome editing which resulted in the reduction of trichome density and length. Another defense is callose synthesis which is controlled by 2 UDP-glucose pyrophosphorylase (UGPase) genes ((UGP1 and UGP2) and 10 glucan synthase-like (GSL) genes (Chen et al. 2006; Shi et al. 2015)) in rice. Ke et al. (2019) using a mutant pex1 (Leucine-rich repeat extensin-like protein), found a higher lignin content and increased expression of lignin biosynthesis genes in this mutant compared to the wild types. This is because the mutant was formed by the ectopic expression of a leucine-rich repeat extension-like gene, OsPEX1 and they observed the reduced lignin content in OsPEX1 suppressed plants confirming the role of OsPEX1 gene in lignin biosynthesis. According to Kawasaki et al. (2006), OsRac1, belonging to GTPases is the enzyme responsible for regulating the lignin deposition in the cells as a defense reaction and this is through the regulation of NADPH oxidase and the activities of cinnamoyl-CoA reductase 1 (OsCCR1) that is an effector of OsRac1. Similarly, another protein, named GLPs (Germin-like proteins), is also responsible for altering the lignin synthesis genes and helps regulate the lignin accumulation in the cell walls (Shanguan et al. 2023). Needless to say, more comprehensive studies incorporating genomics and transcriptomics are needed to elucidate the genetic and molecular networks involved in the physical defense mechanisms in rice.
Conclusion and future perspectives
As discussed in this mini review, plant structural traits such as trichomes, epicuticular wax, silicon, callose deposition, and lignin have crucial roles in reducing insect herbivory in rice. However, these structural traits are not explored and not well understood, especially in the context of rice-herbivore interactions, when compared to their dicot counterparts. Insect herbivory and pesticide resistance development are serious concerns, and are due to the indiscriminate use of chemicals and pesticide residue that affects the quantity and quality of rice, pre and post harvesting. In addition to resistance against insect pests, surface defenses such as trichomes have a crucial role in protecting plants from changing climatic conditions such as extreme temperatures, water stress, and UV irradiation (Hu et al. 2013; Lan et al. 2019). There is a critical need in elucidating the role of each physical barrier in terms of type, structure, mode of action in controlling the invading pests, which has consequences for determining pest control strategies and the development of resistant traits—thus reducing the build-up of chemicals in the field. Just in the case of trichomes, the morphological diversity at genus and species levels in dicots have been found to have functional consequences (Watts et al. 2023) and clearly with current advances in microscopy and imaging techniques, this can be better resolved. The need for more rice and rice-based products is a global concern and hence, rice production can be improved by exploring the mechanisms underlying plant–herbivore interactions and unveiling how rice plants can use their own defense mechanism to cope up this constant and continuous biotic stress. Research on genetic and molecular mechanisms of physical defenses and identifying the genes responsible for the defense mechanisms can be utilized in plant breeding programs to improve the yield minimizing the environmental impacts, thereby managing pests in a sustainable way.
Data availability
Not applicable.
Abbreviations
- HIPVs:
-
Herbivore-induced plant volatiles
- Si:
-
Silicon
- BPH:
-
Brown plant hopper
- JA:
-
Jasmonic acid
- EW:
-
Epicuticular wax
References
Aghaee MA, Godfrey LA (2014) A century of rice water weevil (Coleoptera: Curculionidae): a history of research and management with an emphasis on the United States. J Integr Pest Manag 5(4):D1–D14. https://doi.org/10.1603/IPM14011
Agrawal AA, Fishbein M, Jetter R, Salminen JP, Goldstein JB, Freitag AE, Sparks JP (2009) Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol 183:848–867. https://doi.org/10.1111/j.1469-8137.2009.02897.x
Agren J, Schemske DW (1993) The cost of defense against herbivores: an experimental study of trichome production in Brassica rapa. Am Nat 141(2):338–350
Akinlosotu TA (1977) Outbreak of the rusty plum aphid, Hysteroneurea setariae Th. (Homoptera: Aphididae), on rice (Oryza sativa L.) in Ibadan Nigeria. Ghana J Agr Sci 10(2):149–150
Alhousari F, Greger M (2018) Silicon and mechanisms of plant resistance to insect pests. Plants 7(2):33. https://doi.org/10.3390/plants7020033
Alvi SM, Ali MA, Chaudhary S, Iqbal S (2003) Population trends and chemical control of rice leaf folder, Cnaphalocrocis medinalis on rice crop. Int J Agri Biol 5:615–617
Andama JB, Mujiono K, Hojo Y, Shinya T, Galis I (2020) Non-glandular silicified trichomes are essential for rice defense against chewing herbivores. Plant Cell Environ. https://doi.org/10.1111/pce.13775
Ane NU, Hussain M (2016) Diversity of insect pests in major rice growing areas of the world. J Entomol Zool Stud 4:36–41
Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta Mol Cell Biol Lipids 1734:91–111. https://doi.org/10.1016/j.bbalip.2005.03.001
Ashley TR, Wiseman BR, Davis FM, Andrews KL (1989) The fall armyworm: a bibliography’. Fla Entomol 72(1):152–202. https://doi.org/10.2307/3494982
Awuni GA, Gore J, Cook D, Musser F, Catchot A, Dobbins C (2015) Impact of Oebalus pugnax (Hemiptera: Pentatomidae) infestation timing on rice yields and quality. J Econ Entomol 108:1739–1747. https://doi.org/10.1093/jee/tov123
Backus EA, Serrano MS, Ranger CM (2005) Mechanisms of hopperburn: an review of insect taxonomy, behavior, and physiology. Annu Rev Entomol 50:125–151. https://doi.org/10.1146/annurev.ento.49.061802.123310
Bandong JP, Litsinger JA (2005) Rice crop stage susceptibility to the rice yellow stemborer Scirpophaga incertulas (Walker) (Lepidoptera: Pyralidae). Int J Pest Manag 51(1):37–43. https://doi.org/10.1080/09670870400028276
Barrion AT, Mochida O, Litsinger JA (1982) The Malayan black bug, Seotinophara coaretata (F.) (Hemiptera: Pentatomidae): a new rice pest in the Philippines. Int Rice Res News 7(6):6–7
Bernaola L, Butterfield TS, Tai TH, Stout MJ (2021) Epicuticular wax rice mutants show reduced resistance to rice water weevil (Coleoptera: Curculionidae) and fall armyworm (Lepidoptera: Noctuidae). Environ Entomol 50(4):948–957. https://doi.org/10.1093/ee/nvab038
Bowling CC (1979) Stylet sheath as an indicator of feeding-activity of the rice stink bug (Heteroptera, Pentatomidae). J Econ Entomol 72:259–260. https://doi.org/10.1093/jee/72.2.259
Cardona JB, Grover S, Bowman MJ, Busta L, Kundu P, Koch KG, Sarath G, Sattler SE, Louis J (2023) Sugars and cuticular waxes impact sugarcane aphid (Melanaphis sacchari) colonization on different developmental stages of sorghum. Plant Sci 330:111646. https://doi.org/10.1016/j.plantsci.2023.111646
Catling H, Islam Z, Pattrasudhi R (1987) Assessing yield losses in deepwater rice due to yellow stem borer, Scirpophaga incertulas (Walker) Bangladesh and Thailand. Crop Prot 6(1):20–27. https://doi.org/10.1016/0261-2194%2887%2990023-8
Chander S (1998) Distribution and damage of green-horned caterpillar, Melantis leda ismene in paddy. Ann Plant Prot Sci 6(1):110–112
Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B, Wang Y, Zhao X, Li S, Zhu L (2006) A B-lectin receptor kinase gene conferring rice blast resistance. Plant J 46:794–804. https://doi.org/10.1111/j.1365-313x.2006.02739.x
Cho KS, Kwon M, Cho JH, Im J, Park Y, Hong S, Hwang I, Kang J (2017) Characterization of trichome morphology and aphid resistance in cultivated and wild species of potato. Hortic Environ Biotechnol 58:450–457. https://doi.org/10.1007/s13580-017-0078-4
Chowdhury S, Rao R, Sreedevi K (2011) Taxonomic studies of leafhopper fauna associated with rice ecosystems in Tripura. Curr Biot 4(4):397–404
Chu HF, Teng KF (1950) Life-history of the leafhopper, Cicadella viridis (L.) (Homoptera: Cicadellidae). Ann Ent Sin 1:14–40
Corbett GH, Yusope M (1924) Seotinophara eoaretata (F.) (the black bug of padi). Malays Agric J 12:91–107
Dalin P, Ågren J, Bjorkman C, Huttunen P, Kärkkäinen K (2008) Leaf trichome formation and plant resistance to herbivory. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Berlin, pp 89–105
Djamin A, Pathak MD (1967) Role of silica in resistance to Asiatic rice borer, Chilo suppressalis (Walker), rice varieties. J Econ Entomol 60(2):347. https://doi.org/10.1093/jee/60.2.347
Dravé EH, Laugé G (1978) Study of the action of silica on the wear of the mandibles of the rice moth: Chilo suppressalis (F. Walker) (Lep. Pyralidae Crambinae). Bull Entomol Soc France 83:159–162
Ehleringer J (1982) The influence of water stress and temperature on leaf pubescence development in Encelia farinoza. Am J Bot 69:670–675. https://doi.org/10.1002/j.1537-2197.1982.tb13306.x
Eigenbrode SD (2004) The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthropod Struct Dev 33(1):91–102. https://doi.org/10.1016/j.asd.2003.11.004
Eigenbrode SD, Pillai SK (1998) Neonate Plutella xylostella responses to surface wax components of a resistant cabbage (Brassica oleracea). J Chem Ecol 24:1611–1627. https://doi.org/10.1023/A:1020812411015
FAO (2018) World food and agriculture statistical pocketbook: 2018. Food and Agriculture Organization, Rome
Felton GW, Donato K, Delvecchio RJ, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–3269
Feng Z, Bartholomew ES, Liu Z, Cui Y, Dong Y, Li S, Wu H, Ren H, Liu X (2021) Glandular trichomes: new focus on horticultural crops. Hortic Res 8(1):158. https://doi.org/10.1038/s41438-021-00592-1
Guo J, Xu C, Wu DI, Zhao Y, Qiu Y, Wang X, Ouyang Y, Cai B, Liu X, Jing S et al (2018) Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nat Genet 50:297–306. https://doi.org/10.1038/s41588-018-0039-6
Han Y, Li P, Gong S, Yang L, Wen L, Hou M (2016) Defense responses in rice induced by silicon amendment against infestation by the leaf folder Cnaphalocrocis medinalis. PLoS ONE 11(4):e0153918. https://doi.org/10.1371/journal.pone.0153918
Han YQ, Gong SL, Wen LZ, Hou ML (2017) Effect of silicon addition to rice plants on Cnaphalocrocis medinalis feeding and oviposition preference. Acta Ecol Sin 37:1623–1629
Han Y, Lei W, Wen L, Hou M (2015) Silicon-mediated resistance in a susceptible rice variety to the rice leaf folder, Cnaphalocrocis medinalis Guenée (Lepidoptera: Pyralidae). PLoS ONE 10(4):e0120557. https://doi.org/10.1371/journal.pone.0120557
Hanifa AM, Subramianiam TR, Ponnaiya BWX (1974) Role of silicon in resistance to the leaf roller, Cnaphalocrocis medinalis Guenée in rice. Indian J Exp Biol 12:463–465
Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol Evol Syst 8:157–178. https://doi.org/10.1016/j.ppees.2007.01.001
Hao P, Liu C, Wang Y, Chen R, Tang M, Du B, Zhu L, He G (2008) Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol 146:1810–1820
Hawthorne DJ, Shapiro JA, Tingey WM, Mutschler MA (1992) Trichome-borne and artificially applied acylsugars of wild tomato deter feeding and oviposition of the leafminer Liriomyza trifolii. Entomol Exp 65:65–73. https://doi.org/10.1111/j.1570-7458.1992.tb01628.x
He W, Yang M, Li Z, Qiu J, Liu F, Qu X, Qiu Y, Li R (2015) High levels of silicon provided as a nutrient in hydroponic culture enhances rice plant resistance to brown planthopper. Crop Prot 67:20–25
He J, Liu Y, Yuan D, Duan M, Liu Y, Shen Z, Yang C, Qiu Z, Liu D, Wen P et al (2020) An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. Proc Natl Acad Sci U S A 117:271–277
Heil M (2015) Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annu Rev Entomol 60(1):213–232. https://doi.org/10.1146/annurev-ento-010814-020753
Heinrichs EA, Viajante VD (1987) Yield loss in rice caused by the caseworm Nymphula depunctalis Guenee (Lepidoptera: Pyralidae). J Plant Prot Trop 4(1):169–177
Heinrichs EA, Mochida O (1984) From secondary to major pest status: the case of the insecticide induced rice brown planthopper, Nilaparvata lugens, resurgence. Prot Ecol 7:201–218
Heinrichs EA, Pathak PK (1980) Resistance to the Rice Gall Midge, Orseolia Oryzae in Rice. Int J Trop Insect Sci 1:123–132. https://doi.org/10.1017/S1742758400000278
Hou M, Yang L, Han YQ, Li P (2017) Improved resistance to the brown planthopper in rice plants amended with silicon and the underlying mechanisms. In: Proceedings of the 7th International Conference on Silicon in Agriculture, UAS, Bengaluru, India, 24–28 October 2017
Hou M, Han Y (2010) Silicon-mediated rice plant resistance to the asiatic rice borer (Lepidoptera: Crambidae): effects of silicon amendment and rice varietal resistance. J Econ Entomol 103(4):1412–1419. https://doi.org/10.1603/EC09341
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Ann Rev Plant Biol 59:41–66. https://doi.org/10.1146/annurev.arplant.59.032607.092825
Hu B, Wan Y, Li X, Zang F, Yan W, Xie J (2013) Phenotypic characterization and genetic analysis of rice with pubescent leaves and Glabrous Hulls (PLgh). Crop Sci 53:1878–1886. https://doi.org/10.2135/cropsci2012.09.0522
Jannoey P, Pongprasert W, Lumyong S, Roytrakul S, Nomura M (2015) Comparative proteomic analysis of two rice cultivars (‘Oryza sativa’ L.) contrasting in Brown Planthopper (BPH) stress resistance. Plant Omics 8(2):96–105
Javvaji S, Telugu UM, Venkata RDB, Madhav MS, Rathod S, Chintalapati P (2021) Characterization of resistance to rice leaf folder, Cnaphalocrocis medinalis, in mutant Samba Mahsuri rice lines. Entomol Exp Appl 169:859–875. https://doi.org/10.1111/eea.13082
Jeer M, Telugu UM, Voleti SR, Padmakumari AP (2016) Soil application of silicon reduces yellow stem borer, Scirpophaga incertulas (Walker) damage in rice. J Appl Entomol 141:189–201. https://doi.org/10.1111/jen.12324
Johnson SN, Waterman JM, Wuhrer R, Rowe RC, Hall CR, Cibils-Stewart X (2021) Siliceous and non-nutritious: nitrogen limitation increases anti- herbivore silicon defences in a model grass. J Ecol 109:3767–3778. https://doi.org/10.1111/1365-2745.13755
Johnson Z, Kaur I, Castillo F, Kariyat R, Bandyopadhyay D (2023) Aloe barbadensis rinds employ physical and chemical defense mechanisms against insect herbivores with varying success. Ind Crops Prod 194:116347. https://doi.org/10.1016/j.indcrop.2023.116347
Jones IM, Koptur S, Wettberg EJV (2017) The use of extrafloral nectar in pest management: overcoming context dependence. J Appl Ecol 54:489–499. https://doi.org/10.1111/1365-2664.12778
Juvik J, Stevens M, Rick C (1994) Survey of the genus Lycopersicon for variability in alpha-tomatine content. Hort Sci 17:764–766. https://doi.org/10.1093/jee/87.2.482
Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago
Karban R, Shiojiri K, Takabayashi J (2002) Unidirectional trichomes in rice and prickles in Andropogon virginicus protect meristems from herbivory. Entomol Exp Appl 170:934–940. https://doi.org/10.1111/eea.13212
Kariyat RR, Balogh CM, Moraski RP, Moraes CMD, Mescher MC, Stephenson AG (2013) Constitutive and herbivore-induced structural defenses are compromised by inbreeding in Solanum carolinense (Solanaceae). Am J Bot 100(6):1014–1021. https://doi.org/10.3732/ajb.1200612
Kariyat RR, Smith JD, Stephenson AG, De Moraes CM, Mescher MC (2017) Non-glandular trichomes of Solanum carolinense deter feeding by Manduca sexta caterpillars and cause damage to the gut peritrophic matrix. Proc Biol Sci 22:284. https://doi.org/10.1098/rspb.2016.2323
Kariyat RR, Raya CE, Chavana J, Cantu J, Guzman G, Sasidharan L (2019) Feeding on glandular and non-glandular leaf trichomes negatively affect growth and development in tobacco hornworm (Manduca sexta) caterpillars. Arthropod-Plant Interact 13:321–333. https://doi.org/10.1007/s11829-019-09678-z
Kaufman PB, Dayanandan P, Franklin CI, Takeoka Y (1985) Structure and function of silica bodies in the epidermal system of grass shoots. Ann Bot 55:487–507. https://doi.org/10.1093/oxfordjournals.aob.a086926
Kaur J, Kariyat R (2020) Role of trichomes in plant stress biology. In: Núñez-Farfán J, Valverde P (eds) Evolutionary ecology of plant-herbivore interaction. Springer, Cham
Kawasaki T, Koita H, Nakatsubo T, Hasegawa K, Wakabayashi K, Takahashi H, Umemura K, Umezawa T, Shimamoto K (2006) Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proc Natl Acad Sci U S A 103(1):230–235. https://doi.org/10.1073/pnas.0509875103
Ke S, Luan X, Liang J et al (2019) Rice OsPEX1, an extensin-like protein, affects lignin biosynthesis and plant growth. Plant Mol Biol 100:151–161. https://doi.org/10.1007/s11103-019-00849-3
Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol 143:849–865
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Sci 291:2141–2143. https://doi.org/10.1126/science.291.5511.2141
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328. https://doi.org/10.1146/annurev.arplant.53.100301.135207
Khan MR, Ahmad M, Ahmad S (1989) Some studies on biology, chemical control and varietal preference of rice leaf folder, Cnaphalocrocis medinalis. Pak J Agri Sci 26:253–263
Khetnon P, Busarakam K, Sukhaket W, Niwaspragrit C, Kamolsukyeunyong W, Kamata N, Sanguansub S (2022) Mechanisms of trichomes and terpene compounds in indigenous and commercial thai rice varieties against brown planthopper. Insects 13(5):427. https://doi.org/10.3390/insects13050427
Kraker J, Huis AKL, Heong JCL, Rabbing R (1999) Population dynamics of rice leaf folders and their natural enemies in irrigated rice in Philippines. Bull Entomol Res 89:411–421
Kumar BDJ, Chakravarthy AK, Doddabasappa B, Basavaraju BS (2009) Biology of the rice gall midge, Orseolia oryzae (Wood-Mason) in southern Karnataka. Karnataka J Agric Sci 22(3):535–537
Kvedaras OL, An M, Choi YS, Gurr GM (2010) Silicon enhances natural enemy attraction and biological control through induced plant defences. Bull Entomol Res 100:367–371. https://doi.org/10.1017/S0007485309990265
Lan T, Zheng Y, Su Z, Yu S, Song H, Zheng X, Lin G, Wu W (2019) OsSPL10, a SBP-box gene, plays a dual role in salt tolerance and trichome formation in rice (Oryza sativa L.). G3 Genes Genomes Genetics 9(12):4107–4114. https://doi.org/10.1534/g3.119.400700
Lefebvre T, Charles-Dominique T, Tomlinson KW (2022) Trunk spines of trees: a physical defence against bark removal and climbing by mammals? Ann Bot 129(5):541–554. https://doi.org/10.1093/aob/mcac025
Levin AD (1973) The role of trichomes in plant defence. Q Rev Biol 48:3–15. https://doi.org/10.1086/407484[CrossRef][GoogleScholar]
Li W, Wu J, Weng S, Zhang D, Zhang Y, Shi C (2010) Characterization and fine mapping of the glabrous leaf and hull mutants (gl1) in rice (Oryza sativa L.). Plant Cell Rep 6:617–627. https://doi.org/10.1007/s00299-010-0848-2
Li S, Tosens T, Harley PC, Harley PC, Jiang Y, Kanagendran A, Grosberg M, Jaamets K, Niinemets Ü (2018) Glandular trichomes as a barrier against atmospheric oxidative stress: relationships with ozone uptake, leaf damage, and emission of LOX products across a diverse set of species. Plant Cell Environ 41:1263–1277. https://doi.org/10.1111/pce.13128
Li J, Tang B, Li Y, Li C, Guo M, Chen H, Han S, Li J, Lou Q, Sun W, Wang P, Guo H, Ye W, Zhang Z, Zhang H, Yu S, Zhang L, Li Z (2021) Rice SPL10 positively regulates trichome development through expression ofHL6andauxin-related genes. J Integr Plant Biol 63:1521–1536. https://doi.org/10.1111/jipb.13140
Litsinger JA, Bandong JP, Chantaraprapha N (1994a) Mass rearing, larval behaviour and effects of plant age on the rice caseworm, Nymphula depunctalis (Guenée) (Lepidoptera: Pyralidae). Crop Prot 13(7):494–502. https://doi.org/10.1016/0261-2194(94)90101-5
Litsinger JA, Bumroongsri V, Morril WL, Sarnthoy O (1994b) Rearing, developmental biology and host plant range of the Rice Skipper Pelopidas Mathias (F.) (Lepidoptera: Hesperiidae). Int J Trop Insect Sci 15:9–17. https://doi.org/10.1017/S1742758400016702
Liu J, Du H, Ding X, Zhou Y, Xie P, Wu J (2017a) Mechanisms of callose deposition in rice regulated by exogenous abscisic acid and its involvement in rice resistance to Nilaparvata lugens Stål (Hemiptera: Delphacidae). Pest Manag Sci 73(12):2559–2568. https://doi.org/10.1002/ps.4655
Liu J, Zhu J, Zhang P, Han L, Reynolds OL, Zeng R, Wu J, Shao Y, You M, Gurr GM (2017b) Silicon supplementation alters the composition of herbivore induced plant volatiles and enhances attraction of parasitoids to infested rice plants. Front Plant Sci 8:1265
Louis J, Singh V, Shah J (2012) Arabidopsis thaliana-aphid interaction. Arabidopsis Book 10:e0159
Lu X, Zhang J, Brown B, Li R, Rodríguez-Romero J, Berasategui A, Liu B, Xu M, Luo D, Pan Z, Baerson SR, Gershenzon J, Li Z, Sesma A, Yang B, Peters RJ (2018) Inferring roles in defense from metabolic allocation of rice diterpenoids. Plant Cell 30(5):1119–1131. https://doi.org/10.1105/tpc.18.00205
Lu J, Robert CA, Riemann M, Cosme M, Mène-Saffrané L, Massana J, Stout MJ, Lou Y, Gershenzon J, Erb M (2015) Induced jasmonate signaling leads to contrasting effects on root damage and herbivore performance. Plant Physiol 167(3):1100–1116
Ma JF, Miyake Y, Takahashi E (2001) Silicon as a beneficial element for crop plants. In: Datnoff LE, Snyder GH, Korndörfer GH (eds) Silicon in agriculture. Elsevier, Amsterdam
Mangal S (2000) Bionomics and management of rice whorl maggot-Hydrellia spp. (Diptera: Ephydridae)—a review. Agric Rev 21(2):110–115
Maragesan S, Chellish S (1987) Yield losses and economic injury by rice leaf folder. Indian J Agri Sci 56:282–285
Massey FP, Hartley SE (2008) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol 8:281–291. https://doi.org/10.1111/j.1365-2656.2008.01472.x
Massey FP, Ennos AR, Hartley SE (2006) Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder. J Anim Ecol 75:595–603. https://doi.org/10.1111/j.1365-2656.2006.01082.x
Miles PW (1999) Aphid saliva. Biol Rev Camb Philos Soc 74:41–85
Mishra JS, Poonia S, Choudhary JS, Kumar R, Monobrullah M, Verma M, Malik MK, Bhatt BP (2019) Rice mealybug (Brevennia rehi) a potential threat to rice in a long-term rice-based conservation agriculture system in the middle Indo-Gangetic Plain. Curr Sci 117(4):566–568
Mitani N, Ma JF, Iwashita T (2005) Identification of the silicon form in xylem sap of rice (Oryza sativa L.). Plant Cell Physiol 46(2):279–283. https://doi.org/10.1093/pcp/pci018
Mitku G, Birhan M, Yalew D (2021) Incidence and distribution of rice insect pests and their natural enemies in rice growing area of South Gondar, Ethiopia. Int j Res Stud Agric Sci 8(3):132–139
Mondal HA, Louis J, Archer L, Patel M, Nalam VJ, Sarowar S, Sivapalan V, Root D, Shah J (2018) Arabidopsis ACTIN-DEPOLYMERIZING FACTOR3 Is Required for controlling aphid feeding from the phloem. Department of Entomology, Faculty Publications. https://digitalcommons.unl.edu/entomologyfacpub/645
Mulcahy MM, Wilson BE, Reagan TE (2022) Spatial distribution of Lissorhoptrus oryzophilus (Coleoptera: Curculionidae) in rice. Environ Entomol 51(1):108–117. https://doi.org/10.1093/ee/nvab120
Murungi LK, Kirwa H, Salifu D, Torto B (2016) Opposing roles of foliar and glandular trichome volatile components in cultivated nightshade interaction with a specialist herbivore. PLoS ONE 11(8):e0160383. https://doi.org/10.1371/journal.pone.0160383
Nagoshi RN, Koffi D, Agboka K, Adjevi AKM, Meagher RL, Goergen G (2021) The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo. PLoS ONE 16(6):e0253528. https://doi.org/10.1371/journal.pone.0253528
Nakata Y, Ueno M, Kihara J, Ichii M, Taketa S, Arase S (2008) Rice blast disease and susceptibility to pests in a silicon uptake-deficient mutant lsi1 of rice. Crop Prot 27:865–868. https://doi.org/10.1016/j.cropro.2007.08.016
Nasruddin A (2013) First record of Hysteroneura setariae (Hemiptera: Aphididae) on Rice in South Sulawesi Province of Indonesia. Fla Entomol 96(2):647–648. https://doi.org/10.1653/024.096.0237
Nath RK, Dutta BC (1997) Economic injury level of rice hispa, Dicladispa armigera (Oliv.). J Agric Sci Soc NorthEast India 10(2):273–274. https://doi.org/10.1079/cabicompendium.27270
Nugaliyadde L, Heinrichs EA (1984) Biology of rice Thrips Stenchaetothrips biformis (Bagnall) (Thysanoptera: Thripidae) and a greenhouse rearing technique. J Econ Entomol 77(5):1171–1175. https://doi.org/10.1093/jee/77.5.1171
Oksanen E (2018) Trichomes form an important first line of defence against adverse environment-New evidence for ozone stress mitigation. Plant Cell Environ 41(7):1497–1499. https://doi.org/10.1111/pce.13187
Panda N, Kush GS (1995) Host plant resistance to insects. CAB International, Wallingford
Pashley DP, Sparks TC, Quisenberry SS, Jamjanya T, Dowd PF (1987) Two fall armyworm strains feed on corn, rice and bermudagrass. Louisiana Agric Mag 30:8–9
Patel DT, Stout MJ, Fuxa JR (2006) Effects of rice panicle age on quantitative and qualitative injury by the rice stink bug (Hemiptera: Pentatomidae). Fla Entomol 89:321–327. https://doi.org/10.1653/0015-4040(2006)89[321:EORPAO]2.0.CO;2.[CrossRef][GoogleScholar]
Pathak MD, Khan ZR (1994) Insect pest of rice. International Rice Research Institute, Manila, p 89
Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184(3):644–656. https://doi.org/10.1111/j.1469-8137.2009.03002.x
Philippe RN, Bohlmann J (2007) Poplar defense against insect herbivores. Canad J Bot 85(12):1111–1126. https://doi.org/10.1139/B07-109
Piperno DR (2006) Phytoliths: a comprehensive guide for archaeologists and paleoecologists. Rowman Altamira press, New York, p 238
Portman SL, Kariyat RR, Johnston MA, StephensonAG MJH (2015) Cascading effects of host plant inbreeding on the larval growth, muscle molecular composition, and flight capacity of an adult herbivorous insect. Funct Ecol 29(3):328–337. https://doi.org/10.1111/1365-2435.12358
Punithavalli M, Muthukrishnan NM, Rajkumar BM (2013) Influence of rice genotypes on folding and spinning behaviour of Leaffolder (Cnaphalocrocis medinalis) and its interaction with leaf damage. Rice Sci 20(6):442–450. https://doi.org/10.1016/S1672-6308(13)60154-7
Qi J, Malook SU, Shen G, Gao L, Zhang C, Li J, Zhang J, Wang L, Wu J (2018) Current understanding of maize and rice defense against insect herbivores. Plant Divers 40(4):189–195. https://doi.org/10.1016/j.pld.2018.06.006
Rajamma P, Das NM (1969) Studies on the biology and control of the rice leaf roller cnaphalocrocis medinalis GUEN. Agri Res J Kerala 7(2):110–112
Ramachandran R, Khan ZR (1991) Mechanisms of resistance in wild rice Oryza brachyantha to rice leaf folder Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae). J Chem Ecol 17:41–65. https://doi.org/10.1007/bf00994421
Raupp MJ (1985) Effects of leaf toughness on mandibular wear of the leaf beetle. Plagiodera Versicolora Ecol Entomol 10:73–79
Resende JTV, Maluf WR, Faria MV, Pfann AZ, Nascimento IR (2006) Acylsugars in tomato leaflets confer resistance to the South American tomato pinworm, Tuta absoluta Meyr. Sci Agric 63:20–25. https://doi.org/10.1590/S0103-90162006000100004
Reynolds OL, Keeping MG, Meyer JH (2009) Silicon-augmented resistance of plants to herbivorous insects: a review. Ann Appl Biol 155:171–186. https://doi.org/10.1111/j.1744-7348.2009.00348.x
Rosumek FB, Silveira FAO, de SNeves F et al (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549. https://doi.org/10.1007/s00442-009-1309-x
Sajjan SS, Singh J (1972) Occurrence of horned caterpillar of rice, Melanitis leda ismene (Cramer) Satyridae: lepidoptera on paddy in Punjab. Sci Cul 38(4):215–216
Salim M, Saxena RC (1992) Iron, silica, and aluminium stresses and varietal resistance in rice: effects on whitebacked planthopper. Crop Sci 32:212–219
Sandhu RK, Sarao PS (2021) Evaluation of antixenosis resistance in wild rice accessions against brown planthopper, Nilaparvata lugens (Stål). Int J Trop Insect Sci 41:65–73
Santiago R, Barros-Rios J, Malvar RA (2013) Impact of cell wall composition on maize resistance to pests and diseases. Int J Mol Sci 14(4):6960–6980. https://doi.org/10.3390/ijms14046960
Sasamoto K (1958) Studies on the relation between silica content of the rice plant and insect pests. IV. On the injury of silicated rice plant caused by the rice-stem-borer and its feeding behaviour. Jpn J Appl Entomol Zool 2:88–92
Sen P, Chakravorty S (1970) Biology of Hispa (Dicladispa) armigera Oliv. (Coleoptera: Chrysomelidae). Indian J Entomol 32(2):123–126
ShangGuan X, Qi Y, Wang A, Ren Y, Wang Y, Xiao T, Shen Z, Wang Q, Xia Y (2023) OsGLP participates in the regulation of lignin synthesis and deposition in rice against copper and cadmium toxicity. Front Plant Sci 13:1078113. https://doi.org/10.3389/fpls.2022.1078113
Sharif MK, Butt MS, Anjum FM, Khan SH (2014) Rice Bran: a novel functional ingredient. Crit Rev Food Sci Nutr 54(6):807–816. https://doi.org/10.1080/10408398.2011.608586
Shepard BM, Justo HD, Rubia EG, Estano DB (1990) Response of the rice plant to damage by the rice whorl maggot Hydrellia philippina Ferino (Diptera: Ephydridae.). J Plant Prot Trop 7(3):173–177
Shi X, Sun X, Zhang Z, Feng D, Zhang Q, Han L, Wu J, Lu T (2015) GLUCAN SYNTHASE-LIKE 5 (GSL5) plays an essential role in male fertility by regulating callose metabolism during microsporogenesis in rice. Plant Cell Physiol 56:497–509. https://doi.org/10.1093/pcp/pcu193
Shi JH, Sun Z, Hu XJ, Jin H, Foba CN, Liu H, Wang C, Liu L, Li FF, Wang MQ (2019) Rice defense responses are induced upon leaf rolling by an insect herbivore. BMC Plant Biol 19(1):514. https://doi.org/10.1186/s12870-019-2116-0
Shi J, Song C, Sun Z, Foba CN, Liao A, Zhao P, Jin H, Wang M (2023) Nitrogen and growth stage influence epicuticular wax composition on rice leaf and sheath. ACS Agric Sci Technol 3:413–420. https://doi.org/10.1021/acsagscitech.2c00335
Sidhu JK, Stout MJ, Blouin DC (2013) Performance and preference of sugarcane borer, Diatraea saccharalis, on rice cultivars. Entomol Exp Appl 149:67–76. https://doi.org/10.1111/eea.12111
Snyder GH, Jones DB, Gascho GJ (1986) Silicon fertilization of rice on everglades histosols. Soil Sci Soc Am J 50:1259–1263. https://doi.org/10.2136/sssaj1986.03615995005000050035x
Sogawa K (1982) The rice brown planthopper: feeding physiology and host plant interactions. Ann Rev Entomol 27:49–73. https://doi.org/10.1146/annurev.en.27.010182.000405
Stam JM, Kroes A, Li Y, Gols R, van Loon JJ, Poelman EH, Dicke M (2013) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713. https://doi.org/10.1146/annurev-arplant-050213-035937
Stone BA, Clarke AE (1992) Chemistry and physiology of higher plant 1,3-β-glucanase (callose). In: BA Stone AE Clark, (eds), Chemistry and biology of (1-3)-β-Glucans. La Trobe University Press, Melbourne, pp 365–429
Subbarao DV, Perraju A (1976) Resistance in some rice strains to first-instar larvae of Tryporyza incertulas (Walker) in relation to plant nutrients and anatomical structure of the plants. Int Rice Res Newslett 1:14–15
Sun W, Gao D, Xiong Y, Tang X, Xiao X, Wang C, Yu S (2017) Hairy Leaf 6, an AP2/ERF transcription factor, interacts with OsWOX3B and regulates trichome formation in rice. Mol Plant 10:1417–1433. https://doi.org/10.1016/j.molp.2017.09.015
Swanson MC, Newsom LD (1962) Effects of infestation by the rice stink bug, Oebalus pugnax, on yield and quality in rice. J Econ Entomol 55:877–879. https://doi.org/10.1093/jee/55.6.877
Teotia TPS, Nand S (1966) Bionomics of the rice skipper Parnara mathias Fabricius (Lepidoptera:Hesperiidae). India J Entomol 28:181–186. https://doi.org/10.1079/cabicompendium.39504
Tianpei X, Li D, Qiu P, Luo J, Zhu Y, Li S (2015) Scorpion peptide LqhIT2 activates phenylpropanoid pathways via jasmonate to increase rice resistance to rice leafrollers. Plant Sci 230:1–11. https://doi.org/10.1016/j.plantsci.2014.10.005
USDA (2022) https://fsa.usda.gov/programs-and-services/rice-production-program/index
Varsani S, Grover S, Zhou S, Koch KG, Huang P-C, Kolomiets MV, Williams WP, Heng-Moss T, Sarath G, Luthe DS et al (2019) 12-oxo-phytodienoic acid acts as a regulator of maize defense against corn leaf aphid. Plant Physiol 179:1402–1415. https://doi.org/10.1104/pp.18.01472
Velusamy R (1990) Relative susceptibility of high-yielding rice varieties to the thrips, Stenchaetothrips biformis (Bagnall) (Thysanoptera: Thripidae). Crop Prot 9(3):193–196. https://doi.org/10.1016/0261-2194(90)90163-2
Verma JP, Yadav J, Tiwari KN, Jaiswal DK (2014) Evaluation of plant growth promoting activities of microbial strains and their effect on growth and yield of chickpea (Cicer arietinum L.) in India. Soil Biol Biochem 70:33–37. https://doi.org/10.1016/j.soilbio.2013.12.001
Viajante VD, Heinrichs EA (1986) Rice growth and yield as affected by the whorl maggot Hydrellia philippina Ferino (Diptera: Ephydridae). Crop Prot 5(3):176–181. https://doi.org/10.1016/0261-2194(86)90028-1
Viz JA, Pacada IG (2022) Density, orientation, and distribution of FoliarTrichomes in selected Philippine traditional rice varieties with resistance to Scirpophaga spp. Philipp J Sci 151(5):1737–1745
Wang L, Wu JQ (2013) The essential role of jasmonic acid in plant-herbivore interactions using the wild tobacco Nicotiana attenuata as a model. J Genet Genom 40(12):597–606. https://doi.org/10.1016/j.jgg.2013.10.001
Watts S, Kariyat R (2021) Morphological characterization of trichomes show enormous variation in shape, density, and dimensions across the leaves of 14 Solanum species. AoB Plants 13(6):plab071. https://doi.org/10.1093/aobpla/plab071
Watts S, Kariyat R (2022) Are epicuticular waxes a surface defense comparable to trichomes? A test using two Solanum species and a specialist herbivore. Botany. https://doi.org/10.1139/cjb-2021-0206
Way M (2003) Rice arthropod pests and their management in the United States. In: Smith CW, Dilday RH (eds) Rice: origin, history, technology and production. Wiley, Hoboken, pp 437–456
Werker E (2000) Trichome diversity and development. Adv Bot Res 31(1):1–35. https://doi.org/10.1016/S0065-2296(00)31005-9
White C, Eigenbrode SD (2000) Effects of surface wax variation in Pisum sativum on herbivorous and entomophagous insects in the field. Environ Entomol 29:773–780. https://doi.org/10.1603/0046-225X-29.4.773
Wijayanti RS, Supriyadi PSH (2019) Brown Planthoppers population in local rice varieties based on cellulose, hemicellulose and lignin content. IOP Conf Ser Earth Environ Sci 250:012013. https://doi.org/10.1088/1755-1315/250/1/012013
Will T, van Bel AJE (2006) Physical and chemical interactions between aphids and plants. J Exp Bot 57:729–737. https://doi.org/10.1093/jxb/erj089
Williams DJ, Radunz LAJ, Brook HM (1981) The rice mealybug Brevennia rehi (lindinger) now recorded from Australia and papua new guinea (hemiptera coccoidea: pseudococcidae). J Aust Ent Soc 20:46. https://doi.org/10.1111/j.1440-6055.1981.tb00998.x
Wilson MR, Claridge MF (1991) Handbook for the identification of leafhoppers and planthoppers of rice. CAB International, Wallingford, p 142
Wójcicka A (2015) Surface waxes as a plant defense barrier towards grain aphid. Acta Biol Cracov Bot 57:95–103. https://doi.org/10.1515/abcsb-2015-0012
Woodhead S, Padgham DE (1988) The effect of plant surface characteristics on resistance of rice to the brown planthopper, Nilaparvata lugens. Entomol Exp Appl 47:15–22. https://doi.org/10.1111/j.1570-7458.1988.tb02276.x
Wu JQ, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. https://doi.org/10.1146/annurev-genet-102209-163500
Xiao K, Mao X, Lin Y, Xu H, Zhu Y, Cai Q, Xie H, Zhang J (2017) Trichome, a functional diversity phenotype in plant. Mol Biol 6:183. https://doi.org/10.4172/2168-9547.1000183
Xing Z, Liu Y, Cai W, Huang X, Wu S, Lei Z (2017) Efficiency of trichome-based plant defense in Phaseolus vulgaris depends on insect behavior, plant ontogeny, and structure. Front Plant Sci 8:2006. https://doi.org/10.3389/fpls.2017.02006
Yang GQ, Zhu ZF, Hu WF, Ge LQ, Wu JC (2014) Effects of foliar spraying of silicon and phosphorus on rice (Oryza sativa) plants and their resistance to the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Acta Entomol Sin 57:927–934
Yang L, Han Y, Li P, Wen L, Hou M (2017a) Silicon amendment to rice plants impairs sucking behaviors and population growth in the phloem feeder Nilaparvata lugens (Hemiptera: Delphacidae). Sci Rep 7:1101. https://doi.org/10.1038/s41598-017-01060-4
Yang L, Han YQ, Li P, Li F, Ali S, Hou ML (2017b) Silicon amendment is involved in the induction of plant defense responses to a phloem feeder. Sci Rep 7:4232
Yang L, Li P, Li F, Ali S, Sun X, Hou M (2018) Silicon amendment to rice plants contributes to reduced feeding in a phloem sucking insect through modulation of callose deposition. Ecol Evol 8:631–637. https://doi.org/10.1002/ece3.3653
Ye M, Song Y, Long J, Wang R, Baerson SR, Pan Z, ZhuSalzman K, Xie J, Cai K, Luo S, Zeng R (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci USA 110:E3631–E3639. https://doi.org/10.1073/pnas.1305848110
Zhang Q, Li T, Gao M, Ye M, Lin M, Wu D, Guo J, Guan W, Wang J, Yang K et al (2022) Transcriptome and metabolome profiling reveal the resistance mechanisms of rice against Brown Planthopper. Int J Mol Sci 23:4083. https://doi.org/10.3390/ijms23084083
Zheng X, Xin Y, Peng Y, Shan J, Zhang N, Wu D, Guo J, Huang J, Guan W, Shi S et al (2020) Lipidomic analyses reveal enhanced lipolysis in planthoppers feeding on resistant host plants. Sci China Life 64:1502–1521. https://doi.org/10.1007/s11427-020-1834-9
Zheng Y, Zhang X, Liu X, Qin N, Xu K, Zeng R, Liu J, Song Y (2021) Nitrogen supply alters rice defense against the striped stem borer Chilo suppressalis. Front Plant Sci 12:691292. https://doi.org/10.3389/fpls.2021.691292.PMID:34381479;PMCID:PMC8351598
Zou LI, Stout MJ, Ring DR (2004) Degree-day models for emergence and development of the rice water weevil (Coleoptera: Curculionidae) in Southwestern Louisiana. Environ Entomol 33:1541–1548. https://doi.org/10.1603/0046-225X-33.6.1541
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Balakrishnan, D., Bateman, N. & Kariyat, R.R. Rice physical defenses and their role against insect herbivores. Planta 259, 110 (2024). https://doi.org/10.1007/s00425-024-04381-7
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DOI: https://doi.org/10.1007/s00425-024-04381-7