Introduction
In their natural environment, plants frequently encounter two or more stresses that can limit their productivity and fitness (Spooner, Peralta and Knapp, 2005; Mittler, 2006; Holopainen and Gershenzon, 2010). These include both abiotic stresses (e.g., soil salinization, drought, extreme temperatures, waterlogging) and biotic stresses (e.g., herbivory (insect or mammalian) and pathogen-borne diseases (bacterial, fungal, or viral) (Gull, Lone and Wani, 2019). Plant stress response pathways are dynamic and influenced by diverse factors such as stress type, location, intensity, duration, and the interplay of interacting stresses (Singh, Dhanapal and Yadav, 2020).
The progressive salinization of cultivable land is an abiotic stress that poses a major threat to global agriculture, causing billions of dollars in losses annually (Pitman and Läuchli, 2002; Ashraf, 2010; Ruanet al. , 2010; Jamil et al. , 2011; Munns and Gilliham, 2015). It is estimated that more than 50% of cultivable lands will be salinized by 2050 (Ashraf, 2009; Lakhdar et al. , 2009; Zhaoet al. , 2020). Various natural and anthropogenic factors contribute to soil salinization, including low precipitation, saline groundwater contamination, poor irrigation, and seawater intrusion in coastal areas (Shrivastava and Kumar, 2015; Kaya et al. , 2022; Zhang et al. , 2022; Sahbeni et al. , 2023). Salinity stress impacts plants by reducing water uptake in roots, leading to cell dehydration and increased ionic toxicity by Na+ and Cl- ions that disrupt osmotic balance, ultimately resulting in reduced plant growth and development (Rengasamy, 2006; Munns and Tester, 2008). Salt stress also impairs photosynthesis, leading to decreased carbon fixation and biomass production, and has been documented to compromise plant yields in several crops such as rice, wheat, barley, and tomato (Parida and Das, 2005; Shabala, Wu and Bose, 2015).
Tomato plants are affected under conditions of high salinity, leading to reduced seed germination and fruit yields (Cuartero et al. , 2006). However, some tomato plants are known to be moderately salt sensitive and certain varieties can exhibit salt tolerance properties (Hayward and Long, 1943; Spooner, Peralta and Knapp, 2005; Martinezet al. , 2012; Guo et al. , 2022). This variation in salt tolerance among tomato cultivars can be attributed to differential expression of specific genes and proteins that regulate homeostasis and stress responses, including the high-affinity K+/ Na+ transporter (HKT1like transporters) (Rubio, Gassmann and Schroeder, 1995; Nieves-Cordones et al. , 2008; Zhanget al. , 2008, 2018), vacuolar Na+/ H+ antiporters (NHX1-like transporters) that mediate Na+ extrusion and sequestration to vacuoles (Apseet al. , 1999; Serrano and Rodriguez-Navarro, 2001; Rodríguez‐Rosales et al. , 2008; Wang et al. , 2020; Soliset al. , 2022), and the abscisic acid-responsive element binding protein (AREB1 family) (Seok et al. , 2017; Yoo et al. , 2019). Simply put, plants deal with ionic stress by Na+ exclusion, Na+ inclusion and sequestration into vacuoles, or via tissue tolerance. The mechanism of salt tolerance at play depends on the plant species or variety and can lead to varying plant tissue contents based on the mechanism.
Furthermore, excessive salt can trigger the accumulation of reactive oxygen species (ROS). Low ROS concentrations can be involved in signal transduction (Miller et al. , 2010), whereas high ROS concentrations can lead to oxidative stress and damage to cellular components such as proteins, lipids, and DNA (Provin and Pitt, 2001; Foolad, 2004; Yang and Guo, 2018). Higher amounts of H2O2 and ROS species are commonly seen in plant responses to biotic stress, such as insect herbivory. H2O2 accumulation has been reported in salt-stressed maize and tomato plants at 24 and 48 hours post-salt application (Forieri, Hildebrandt and Rostás, 2016; Tandra et al. , 2022). A study reported that ROS accumulation under salt stress primed a JA-mediated anti-insect herbivory defense response (Sabina and Jithesh, 2021). As salt stress and herbivory co-occur, plant responses to one stress will have implications for cross-tolerance to another (Capiati, País and Téllez-Iñón, 2006; Fujita et al. , 2006).
Herbivorous pests devour plant tissue, reduce the plant’s photosynthetic capacity, and alter plant metabolism, nutrient acquisition and allocation, thus impacting crop yields (Babst et al. , 2008; Qu, 2019). The corn earworm caterpillar (Helicoverpa zea ) is one of the most destructive pests of tomatoes, corn, and cotton, causing annual losses exceeding $1 billion globally (Wilcox, Howland and Campbell, 1956; Capinera, 2000; Blanco et al. , 2007; Rhino et al. , 2016; da Silva et al. , 2020). H. zea is known to trigger ROS accumulation and activate the JA-dependent plant defense response pathway in cotton (Bi, Murphy and Felton, 1997) and soybean (Bi and Felton, 1995). The JA-dependent plant defense response alters the production of plant defense metabolites, including alkaloids and protease inhibitors (Wang et al. , 2019; Jiao et al. , 2022).
Plants use distinct response pathways for individual stressors. However, plants under multifactorial combinations often exploit overlapping and converging pathways via shared proteins or signaling molecules to mount more efficient responses (Sewelam, Kazan and Schenk, 2016).However, the specificity of plant responses to unique stress combinations hinders our comprehensive understanding of their complex interplay and emergent outcomes. It thus becomes difficult to predict how plants will respond to multiple stresses. Furthermore, the performance of herbivorous pests feeding on stressed plants is influenced by plant quality, nutrient composition, and defense chemical levels that can be influenced under stress (Ali et al. , 2021). The plant stress hypothesis predicts that stressed plants should have higher herbivore abundance due to a decreased concentration of defense chemicals or changes to plant nutrient: chemical defense ratios (White, 1969, 1984; Joern and Mole, 2005). Conversely, the plant vigor hypothesis predicts that healthier plants (or plant parts) exhibit higher vigor and are better hosts for herbivores than stressed plants due to the higher availability of nutrients (Price, 1991; Cornelissen, Wilson Fernandes and Vasconcellos‐Neto, 2008).
The effects of salinity stress on insect herbivores depend upon the specific host plant-insect interaction.
The responses of herbivorous pests to changes in plant quality can vary both within and among feeding guilds (Awmack and Leather, 2002; Huberty and Denno, 2004). Some studies have demonstrated that increased salinity levels can enhance insect pest performance on host plants. Leaf miner (Tuta absoluta ) development rates on tomato plants have been shown to increase under saline conditions (Han et al. , 2016). Another study on the two-spotted spider mite (Tetranychus urticae ) showed positive correlations between mite fecundity and population growth on soybean (Glycine max ) and maize (Zea mays ) to salt stress (Eichele-Nelson et al. , 2017). Green peach aphid (Myzus persicae ) abundance increased on sweet pepper plants (Capsicum annuum ) under saline conditions (Polack, Pereyra and Sarandón, 2011). However, some studies show that increased salinity levels decrease herbivore performance on plants. Brown planthopper (Nilaparvata lugens ) survival parameters such as nymphal development period, adult longevity and oviposition, and population density on rice (Oryza sativa ) decreased due to lower plant quality (Quais et al. , 2019; Ali et al. , 2021). A study on wheat showed that the survival parameters of the cherry-oat aphid (Rhopalosiphum padi ) were negatively affected by salt stress (Ghodoum Parizipour et al. , 2021). The soybean looper (Pseudoplusia includens ) showed lower growth in salt-exposed soybean chloride-includer varieties (Najjar et al. , 2018). Literature focusing on salinity stress effects on plant-chewing-insect interactions seems to be highly variable and limited.
Just as plant quality determines insect performance, it also impacts the release of plant volatile organic compounds (VOCs) (Holopainen and Gershenzon, 2010). A study on salt-treated maize reported decreased VOC emissions per plant but not per biomass (Forieri, Hildebrandt and Rostás, 2016). They also observed differential emission of specific VOCs between salt treatments. Plant VOC emissions are used as signals for host selection by moths and can also influence higher tropic levels (Bernays and Chapman, 2007; Karban, 2008; Ninkovic, Markovic and Rensing, 2021). Many times, the establishment of insect pests on a plant begins with an adult moth perceiving appropriate hosts via VOCs and laying its eggs on the host plant (Penaflor et al. , 2011). Therefore, along with assessing caterpillar performance on plants, it becomes necessary to investigate moth oviposition preferences to get a comprehensive idea of the plant-insect interaction at play.
In this paper, we discuss tomato (Solanum lycopersicum ) responses to combined stresses of salinity (NaCl) and insect herbivory by the generalist polyphagous corn earworm caterpillar Helicoverpa zeaBoddie (Lepidoptera: Noctuidae) (Quaintance and Brues, 1905; Fitt, 1989). We hypothesized that salt-treated plants would negatively affectH. zea caterpillar performance and influence their foraging and oviposition behavior. We also speculated that this effect might be influenced by several factors, including reduced water content in plants, decreased total protein levels, ionic toxicity, nutrient imbalances, heightened levels of proteins that defend against herbivores, changes in volatile organic compound (VOC) emissions, or a combination of these elements.