Elevated CO₂ and Temperature Resetting the Expression of Resistance, Pest Incidence, Geographical Distribution and Physiology in Insect-pests of Grain Legumes: A Review

CO₂ level in the atmosphere is currently about 406.94 parts per million (ppm) on a worldwide scale (Anon, 2017). In the last 250 years, atmospheric CO₂ concentration has risen from 280 to 390ppm and by the end of 2050, it expected to rise at least 550ppm (IPCC, 2007). As an abiotic element, it affects the expression of plant resistance (Lindroth, 2010; Robinson et al., 2012). Elevated level of CO₂ increases the C:N ratio, which lowers the nitrogen concentration in the tissues of most plant species, making them more sensitive and affecting the feeding habits of insect-pest species (Bezemer et al., 2000; Sun et al., 2010; Couture et al., 2010; Guo et al., 2014). To balance this ration, the phytophagous animals would consume more foliage and therefore, more damage to crop plants (Bezemer and Jones, 1998). Variations in climatic change have a significant impact on pest abundance and dispersion (McKenzie and Andrews, 2010; Sharma, 2014). Alteration in CO₂ concentration also results in biochemical and morphological changes (Robinson et al., 2012) and that plays vital role in plant defence mechanism of host plant resistance to insect pests (War et al., 2012, 2013). Generally the plant develops many strategies to defend itself against the negative impacts of foliar feeders (Strauss and Agrawal, 1999; Fornoni et al., 2003). Plants respond by producing repellents or defensive elements so to reduce the effect of pest species (Halitschke and Baldwin, 2004). Elevated CO₂ also alters the activity of plant oxidative enzymes such as peroxidase (POD), polyphenol oxidase (PPO), phenylalanine ammonia lyase (PAL), tyrosine ammonia lyase (TAL), superoxide dismutase and catalase in the host plant (Badiani et al., 1993; Polle et al., 1997). The photosynthetic rate, which is regulated by ambient CO₂ level, has a significant impact on the physiology and biochemical composition (C:N ratio) of plant foliage, as well as the allocation of these components of plant leaves (Long et al., 2004). When wild tomato plants are grown and fed under elevated CO₂, the activities of total protease, trypsin-like enzymes and weak and active alkaline trypsin-like enzymes increased in the midgut of the cotton bollworm, Helicoverpa armigera (Hubner) (Guo et al., 2012). The negative impact of elevated CO₂ level on insect physiology has been investigated (Akbar et al., 2016). The development and physiology of herbivorous insects are affected by the changes in food quality (Khadar et al., 2014). Sharma et al., (2016a) investigated the effect of increased CO₂ on plant defense response in chickpea against Helicoverpa armigera and found increase in total phenols and condensed tannins. Tannins in plant foliage can protect against foliage feeder by making the plant toxic or deterring the insects from feeding on it (Barbehenn and Constabel, 2011). Hydrogen peroxide, oxalic and malic acid level were higher in H. armigera-infested plants at 750 ppm than at 350 ppm CO₂ level (Sharma et al., 2016b). The primary goal of this review paper was to determine the impact of increased CO₂ concentration and temperature on resistance expression, pest damage and insect development in grain legumes.
 
Elevated CO₂­ and temperature vs pest incidence and geographical distribution
 
According to the third IPCC study, global average surface temperature is expected to rise by 1.4°C to 5.8°C by 2100 and after it will rise even more fast (Houghton et al., 2001). During the last 1,000 years, the rise in temperature in the twentieth century has been the most serious problem of any century. As a result of global warming, pest outbreak have become more common and severe (Sharma, 2014). The pest population became unstable due to rising CO₂ level and resulted in severe outbreak of pest species (War et al., 2016). Regional distribution, abundance, seasonal incidence and intensity of few pests got shifted due to elevated CO₂ level (Menendez, 2007; IPCC, 2014; Sharma, 2014). Change in climate fastens the severe outbreak of H. armigera and Maruca vitrata in legume crops (Sharma, 2005; Sharma, 2010). Among all the abiotic climatic variations, the extreme range of temperature has a significant impact on phytophagous herbivore distribution (Boullis et al., 2015). More potential of new pests and pest niches arise when the average temperature rises. Pod infestation by H. armigera and M. vitrata in pigeonpea crops varies and it depends the temperature at different planting dates (Jat et al., 2021; Jat et al., 2018a) (Table 1). In the pigeonpea crop, higher temperature results in a greater larval population as well as a higher incidence of H. armigera and M. vitrata. The larval population of H. armigera was positively correlated with the higher temperature (Jat et al., 2017). Furthermore, the occurrence of insect pests in pigeonpea and chickpea crops also varied in different months (Sharma et al., 2016b). In September and January seeded pigeonpea and chickpea crops, the crop damage was appreciably high due to infestation by H. armigera and Spodoptera exigua (Hub.) (Sharma et al., 2016b).


 
Effect of elevated CO₂ and temperature on foliage consumption and insect development
 
Nitrogen is one of the most critical limiting factors for phytophagous herbivores (Mattson, 1980). Decrease in the foliar nitrogen content of the host plant may impair the development and survival rates of phytophagous insects. Variability in climatic variables weakens the plant’s defence against herbivorous insects by virtue of the fact that nitrogen is the most abundant component of proteins (Khadar et al., 2014; Sharma, 2016) and a limiting element for insect-pest reproduction and performance (Lindroth et al., 1993; Shwetha et al., 2019). Therefore, decrease in leaf nitrogen content under elevated CO₂ concentration results in plant nitrogen deficit (Lindroth et al., 1993). Feeding such plants would enhance the leaf consumption and duration of development (Feng et al., 2010). For instance, the chickpea plant grown in high CO₂ concentration has decreased protein content in their tissues, making them nutritionally deficient (Khadar et al., 2014). H. armigera needs more protein for proper growth and development and it will strive to compensate by consuming as much as possible. Carbon dioxide also reduced the plant’s ability to defend itself against phytophagous insects (Zavala et al., 2008). Coviella and Trumble (1999) and Sharma et al., (2016b) hypothesized that plants grown under higher CO₂ and temperature level are less nutritious and herbivores will increase their feeding time and foliage consumption.
       
Insect development and physiology directly influenced by temperature fluctuations, with equivalent impacts on the nutritional composition of host plants (Ayres and Scriber 1994). Hunter (2001) and Yadugiri (2010) investigated the direct and indirect effects of temperature and CO₂ on insect growth. In general, rising temperature leads to a higher survival rate and a shorter life cycle (Bale et al., 2002). Increasing in plant dry biomass and C:N ratio, longer main stem length, elongation of branches, individual leaf area per plant and reduced foliar nitrogen are the results of increased CO₂ sensitivity in C₃ plants (Chen et al., 2005a; Shwetha et al., 2019). Increased CO₂ (550ppm) results in significantly greater leaf area, root dry weight and total dry matter accumulation in French bean plants (Rao et al., 2015). Because of CO₂ fixation mechanisms, leguminous crops respond positively to elevated CO₂ level and results in increased biomass output among C₃ plants (Kimball et al., 2002). Some mungbean genotypes have a beneficial attributes with increased CO₂ concentrations (570-20ppm) (Haque et al., 2005).
       
The drop in leaf N content caused by quicker growth of the foliage plants stimulated photosynthesis and growth in plants growing under elevated CO₂ circumstances (Stitt and Krapp, 1999). Under high CO₂, the leaf N content of legume crops reduced by an average of 7% (Cotrufo et al., 1998). Rao et al., (2012) found an 8% drop in leaf N content under increased CO₂ concentrations when compared to ambient CO_2. The foliar nitrogen concentration of the plant decreases as CO₂ level rises and results in 40% higher food consumption by herbivores (Sharma et al., 2016b; Chen et al., 2005b).
       
The nutritional composition of the plant became altered by increased CO₂ concentration and temperature, which might make the foliage plant unpleasant or nutritionally better for the insects (Sterner and Elser, 2002). Lower level of leaf nitrogen, higher carbon, higher relative proportions of carbon to nitrogen and higher polyphenols content have been recorded in groundnut plants cultivated under elevated eCO₂ (550 ppm and 700 ppm) level. When compared to ambient CO₂ level, leads to longer larval duration, greater larval weight and increase intake of groundnut plant leaf (Rao et al., 2012; 2014). Similarly, groundnut foliage grown in eCO₂ circumstances has reduced leaf nitrogen content, greater carbon and a higher C:N ratio (Shwetha et al., 2019).
       
Increased temperature causes a faster rate of development in arthropods and results in more generations per year and a wider geographical dispersion (Parmesan et al., 1999; Bale et al., 2002; Sharma 2014). When Helicoverpa armigera larvae were reared under elevated CO₂, larval survival, larval weight, larval period, pupation and adult emergence were all negatively affected, whereas pupal weight, pupal period and adult fecundity were improved (Akbar et al., 2016). In brief, the growth and development, reproduction and survival of of H. armigera, were strongly influenced by rising temperature and precipitation (Sharma, 2014). Similarly, when the larvae of Spodoptera litura feed on groundnut plants with eCO₂ values (550 ppm and 700 ppm), showed a longer larval duration and larval weight (Rao et al., 2014). On the contrary, with elevated CO₂ concentrations (732.1±9.99 µl/liter), larval and pupal weights of S. litura were significantly reduced, but the duration of larval and pupa on soybean were significantly increased (Yifei et al., 2018).
       
Adati et al., (2004) investigated the effect of temperature on the development and survival of the legume pod borer, Maruca vitrata, under the in vivo condition. The developmental time for eggs, larvae and pupae reduced with increasing temperature from 14.4°C to 29.3°C. For development of egg, larval and pupal stages, the thermal constant and lower thermal threshold were 51.1, 234.7 and 116.5 degree-days and 10.5, 10.0 and 10.9°C, respectively.
       
The aphid population on soybean plants was considerably greater after 1 week under elevated CO₂ (550 L/L) concentrations, with populations twice the size of plants cultivated under ambient CO₂ level (O’Neill et al.,  2011). Similarly, higher temperature has a detrimental impact on larval survival, larval duration, pupal weight and pupal period, but has a positive impact on larval growth. Increased metabolic rate may be responsible for increased larval growth (Bale et al., 2002; Jamieson et al., 2012). Increased food consumption and metabolism of H. armigera larvae were observed when CO₂ and temperature levels were enhanced (Akbar et al., 2016). This is due to increased activity of midgut protease, amylase and cellulose (carbohydrates) and mitochondrial enzymes. When larvae were reared under elevated CO₂ concentration compared to ambient CO₂ level, Khadar et al., (2014) found that food consumption rose by 81.67 percent. The food consumption of S. litura was maximum (3758.07 mg) during its whole life cycle when exposed to eCO2 + eTemperature (550 ppm + 2^oC) (Shwetha et al., 2019). In line, Wu et al., (2006) observed similar observations. Yifei et al., (2018) proposed that elevated CO₂ level promote an increase in the amount of feeding and excretion of soybean plants by S. litura.
       
Chickpea plants cultivated at high CO₂ level (550 ppm and 700 ppm) exhibited low nitrogen and high carbon content and that has led to increased food consumption by H. armigera, which in turn increased larval weight and increased the excreta (Khadar et al., 2014). More damage to chickpea plants is the result of no change in phenol content, more approximate digestibility and more relative consumption rate by the larva under elevated CO₂ as compared to ambient CO₂ level. The nutritional quality of mungbean leaves was reduced due to dilution of nitrogen content under elevated CO₂ level, resulting in increased feeding capacity of S. litura (Srivastava et al., 2002). As atmospheric CO₂ level goes up, it may decrease nitrogen concentration and high non-structural carbohydrate level. This climatic change may alter the plant-herbivore interaction, as well as S. litura feeding habits.
 
Elevated CO₂ vs change in morphological and biochemical components
 
Hunter (2001) has clearly established the effect of increased CO₂ concentration on plant phytochemistry. Climate change, particularly changes in CO₂ and temperature regimes have a significant impact on host-plant resistance mechanisms (Sharma et al., 2016b) (Table 2 and 3). The photosynthetic route determines the growth and development as well as the biochemical contents of plants cultivated in high CO₂ environment. Groundnut and chickpea plants grown in CO₂ (550 ppm) had a considerable drop in leaf nitrogen and protein, whereas the carbon C:N ratio, phenols and tannin content were much greater in CO₂ (550 ppm) and least in ambient concentration (Shwetha et al., 2019; Khadar et al., 2014). Elevated temperature seems to reduce the morphological and biochemical components of the pigeonpea resulting in increasing damage by pod borer (Jat et al., 2018a; Jat et al., 2021). (Table 4). In comparison to June sown pigeonpea genotypes to July or August sown genotypes, the phenol content and condensed tannins were found higher (Jat et al., 2018b) (Table 5 and 6). Such changes have led to the pod borer infestation in the pigeonpea. The mean phenol content of chickpea plants infested with H. armigera was substantially higher than that of uninfested plants (Sharma et al., 2016b). Under elevated CO₂ concentration (550 and 750 ppm), the activity of phenylalanine ammonia lyase (PAL), tyrosine ammonia lyase (TAL), total phenols and condensed tannins were increased in chickpea plants (Muzika, 1993; Sharma et al., 2016b). Increasing activity of these compounds affects the expression of plant resistance to foliage feeders. Several studies have found that high temperature diminish the expression of genes influencing wheat resistance to several biotypes of the Hessian fly, Mayetiola destructor (Tyler and Hatchett, 1983). Certain environmental conditions, particularly temperature, have an impact on the success of transgenic crops in pest management (Sharma 2014). This elevated condition changes the interaction between insect pests and their host plants.










       
Increased CO₂ concentration could reduce photorespiration in C₃ photosynthesis and makes photosynthesis more efficient. But the foliar nitrogen and protein concentrations dropped more than 12% (Ainsworth and Long 2005). According to Dermody et al., (2008) higher CO₂ level alone and in combination with O₃ increased the abundance of western corn rootworm, Diabrotica virgifera adults (foliage chewer) and soybean aphids, Aphis glycines (phloem feeder), as well as the amount of leaf area damage in the soybean agroecosystem. At excessive CO₂ concentration (550), the Japanese beetle, Popillia japonica, significantly increased the foliage damage to soybean plants. Maximum consumption of leaf was observed among the beetle was observed when the temperature was raised to 37° C (Niziolek et al., 2013). The nutritional value of plants is greatly reduced due to loss of nitrogen and protein, influencing the growth and development of insect herbivores either directly or indirectly. On the other hand, plants using C4 pathway of photosynthesis will have poor response to increased atmospheric CO₂ due to photosynthetic saturation (Leon and Vara, 2004).
 
Effect of elevated CO₂ and temperature on resistance resetting
 
Many studies have observed association between herbivore tolerance and resistance (Bailey and Schweitzer, 2010), but little is known about how abiotic factors like global CO₂ and temperature affect the relationship between tolerance and resistance. According to Guo et al., (2012) elevated CO₂ reduces tomato plant resistance to H. armigera by suppressing the critical defensive signal molecule JA and JA-pathway-related defensive enzymes. Tomato plants grown in elevated CO₂ are also less tolerant to H. armigera than plants grown in ambient CO₂. Raised CO₂ concentration produce higher leaf glucose concentration and lowered nitrogen content when combined with increased temperature (DeLucia et al., 2012). Both alterations in plant foliage reduce the plant’s nutritional value, causing certain herbivores to consume more leaves to meet their nutritional requirement. Srivastava et al., (2002) observed the effect of long-term CO₂ enrichment on mungbean leaf chemistry. According to the above said researchers, under enriched CO₂ (600±50 µl l-1) condition, foliage protein and non-protein nitrogen level decrease whereas, starch and total soluble sugar level of the leaves increase, resulting in more damage by Spodoptera litura damage. The change in herbivore feeding behavior caused by enhanced CO2 has led to considerable ecological disruption. Moreover, high CO₂ level lowers the titre of plant defense hormone jasmonic acid (JA) and promote the production of salicylic acid (SA), these changes in plant hormones could potentially increase sensitivity to chewing insects (DeLucia et al., 2012).

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Not all plant species respond identically to elevated concentrations of CO₂ (Lindroth et al.,  1993). For example, elevated CO₂ results in reduced in foliar nitrogen levels and increased condensed tannin levels in paper birch and but not in white pine (Roth and Lindroth, 1994). Chickpea plants reduce nitrogen-based defensive chemicals (e.g., alkaloids) when CO₂ level rose (Sharma et al., 2016b). Reduced resistance in wild tomato plants when grown under high CO₂ condition. When wild type tomato plants were infested with H. armigera larvae, the levels of jasmonic acid and the activities of lipoxygenase, proteinase inhibitors and polyphenol oxidase were found to be less (Guo et al., 2012) (Fig 1). The expression of resistance and tolerance to the test bug were highest in wild type plants under ambient CO₂ level. Increase in susceptibility of soybean plant to Japanese beetle, Popillia japonica, by lowering the expression of genes related to the defense hormones (jasmonic acid and ethylene). It decreases the gene expression and activity of cysteine proteinase inhibitors (CystPIs), which are the main anti-herbivore defense in plants (Zavala et al., 2010). Jasmonic acid lowered the efficiency of soybean plants when CO₂ level were high (Zavala et al., 2008). Similarly, increase of CO₂ levels affects the amounts of malic and oxalic acid in chickpea plants, thereby reduce the plant resistance mechanisms against herbivores (Selvaraj et al., 2013; Sharma et al., 2016b). Plants that grow under elevated levels of CO₂ are more sensitive to the Japanese beetle, P. japonica and the western corn rootworm, D. virgifera (Zavala et al., 2008). The synthesis of cysteine proteinase inhibitors (CystPIs) was reduced due to the down regulation of defense signaling genes (lipoxygenase 7 (lox7), lipoxygenase 8 (lox8) and 1-amino cyclopropane-1-carboxylate synthase (acc-s). These are the principal coleopteran herbivore deterrent chemicals in soybean. On the contrary, when the plants were infested by P. japonica, ethylene synthesis in healthy plants increased due to higher CO₂ level but reduced the expression of genes in the ethylene-signaling pathway (Casteel et al., 2008).
       
Pigeonpea plants with the shortest incubation period of 18 hours suffered the most Phytophthora cajani infection when grown under 30°C and 85 % RH (Jadesha et al., 2019). Similarly, Pande and Sharma (2010) found a higher incidence of phytophthora blight disease when temperature was 28-30°C and relative humidity was between 75 and 96% inferring that. High temperature seems to reduce plant disease resistance, immunity (Dropkin, 1969) and defensive response, making the plant more susceptible to pathogens (Zhu et al., 2010).

Phytophagous herbivores’ interactions with host plants are unquestionably influenced by changing environmental conditions. In general, increased level of CO₂ concentration and temperature interfere with pest–plant interactions. Pest distribution and severity, foliage composition (which determines pest damage) and the physiology and development of foliar feeder herbivores are determined by these parameters. Elevated CO₂ alters C and N-based molecules, phenolic components and tannins present in the plants, reducing their resistance mechanisms. The net result is such that the plants become susceptible to pest on one hand and the insect multiplies beyond the economic threshold level and bring down the legume yield drastically.