Abstract
Plants respond and adapt to various environmental conditions through morphological, anatomical, and physiological adaptations at the cellular and plant level. These morphological, anatomical, and physiological adaptations help the plant to cope up with the environmental variations and the stress created by those variations. Among these adaptations, morphological and physiological adaptive traits are the most well-studied traits in most crops, including model crops. Drought and salinity stresses are the major abiotic stress factors affecting yield loss worldwide. Sugarcane with 12–18 months of crop cycle is not flexible enough to avoid unfavorable environmental conditions and faces all climatic variability throughout the year. In sugarcane development, about 80% of the sugar accumulates during tillering and grand growth period. Abiotic stresses during these growth stages critically affect sugarcane yield. Both leaf and root anatomical plasticity in crops play an important role in imparting tolerance to various abiotic stresses such as drought, salinity, oxidative stress, high and low temperature. An increase in the leaf cuticle thickness and increase in leaf epidermal thickness are reported to be the anatomical traits in drought-tolerant sugarcane varieties. Intact bulliform cells, bulliform cell area, chloroplast content, and chloroplast ultrastructure, especially the length, width, and width/length of chloroplasts, are reported to be effective indexes for drought-resistant sugarcane variety. Roots are the actual site that requires the highest plasticity during drought combined with high temperature to ensure continuous water movement through the soil-plant-atmosphere continuum. The efficiency of soil water uptake by the root system determines the rate of transpiration and above-ground performance. Increased root length, reduced cortical layer, increased protoxylem poles, increased metaxylem vessels, and reduced metaxylem diameter, which provides better hydraulic resistance, are some of the adaptive root traits reported in sugarcane under drought conditions. This chapter provides an overview of these leaf and root anatomical traits conferring tolerance to various abiotic stresses in sugarcane.
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6.1 Introduction
Sugarcane (Saccharum officinarum L.) (Poaceae) is an economically important crop used for approximately 80% of sugar production globally. Due to the high biomass production, sugarcane is also increasingly used as a source of bioenergy crop. However, a lack of water often limits sugarcane production, specifically at the critical growth stages such as formative and grand growth stages (Naik 2001; Silva et al. 2008; Tammisola 2010; Verma et al. 2019a, b, 2021a, b, c). In India, sugarcane cultivation is experiencing drought in tropical and subtropical regions and depends on supplementary irrigation for growth.
Abiotic stress is a recurrent problem in sugarcane that affects the quantity and quality of its yield. It is estimated that about 2.94 lakh ha is affected by drought in India, and about 2.5 lakh ha is affected by waterlogging (Misra et al. 2020), while nearly 9 mha sugarcane area is reported to be affected by salinity (Brindha et al. 2019). These abiotic stresses disturb the metabolism, growth, and development of sugarcane crop and finally leads to yield loss (Shrivastava and Srivastava 2016; Verma et al. 2020a, b, 2021d). Drought stress is one of the most destructive among all abiotic stresses since sugarcane is known to be a water-loving crop (Zingaretti et al. 2012; Lakshmanan and Robinson 2013; Verma et al. 2021c). Drought stress simultaneously affects several morphological and physiological traits in sugarcane, thereby causing the reduction in overall growth and crop productivity (Yardanov et al. 2003). Sugarcane needs a lot of water during the tillering and grand growth phase (Ramesh 2000). Plants have evolved to adapt to any stress conditions through various morphological, anatomical, and physiological mechanisms. Understanding these mechanisms will not only provide clues towards the crop adaptation to various stress conditions, but it will also help us develop improved tolerant genotypes (Chandler and Bartels 2008; Verma et al. 2019a).
The structural adaptations through leaf and root anatomical features help the plant respond and adapt to limited resources (Matsuda and Rayan 1990). The structural transformations in the leaf are more crucial for plants to survive under drought conditions, which help the plant to protect the photosynthetic machinery and minimize water loss under drought. Adaptive anatomical features of leaves are directly linked to CO2 assimilation rates and photosynthetic efficiency (Terashima et al. 2001). Some leaf traits such as leaf area are reported to contribute to yields in sugarcane directly. Leaf area is another essential characteristic to maximize solar radiation interception and is directly associated with carbon fixation (Sinclair et al. 2004). However, the root is the first organ to sense and respond to water dehydration in soil (Ferreira et al. 2017). Due to their functions in nutrient and water uptake, the anatomical adaptations among root traits also play an important role in determining sustainable yield under stress.
6.2 Leaf Anatomy and Drought Tolerance
Any stress condition impacts the internal structure, reflecting the poor physiological performance of a crop (Pan et al. 2011). The leaf is the first organ to reflect physiological performance, and leaf anatomy and physiology directly correlate with plant drought resistance (Wang et al. 2006). Table 6.1 summarizes the leaf anatomical features studied so far and reported to be important markers for drought resistance in sugarcane.
6.3 Stomatal Density and Size
Stomata with a pair of specialized guard cells surrounding a central pore provide access to the mesophyll cells (Grantz et al. 1987). Stomata play a crucial role in regulating water use and carbon uptake; hence stomatal structures are most extensively studied for plant water use efficiency and drought tolerance (Grantz et al. 1987; Bertolino et al. 2019; Hetherington and Woodward 2003).
Stomatal conductance is regulated in plants through substantial crosstalk between guard cell turgor pressure and stomatal pore aperture movement (Grantz et al. 1987; Kollist et al. 2014). Under reduced soil moisture, high temperature, or light intensity, the guard cell turgor pressure decreases, which results in reduced stomatal aperture and conductance (Schroeder et al. 2001; Mustilli et al. 2002; Tombesi et al. 2015; Bartlett et al. 2016; McAdam and Brodribb 2016). By reducing the stomatal aperture and conductance, plants improve water conservation, but often at the expense of reduced photosynthesis (Flexas and Medrano 2002).
Although the stomatal aperture is significant for stomatal conductance and photosynthesis under water-limiting conditions, stomatal density and stomatal size play an important role (Bertolino et al. 2019; Verma et al. 2020). Stomatal density and size have shown correlation to drought resistance in sugarcane (Zhang et al. 2015). Due to reduced stomatal size, loss in stomatal conductance has been linked to higher water conservation under water deficit conditions (Zhang et al. 2003). Verma et al. (2020) have reported reductions in the stomatal density and stomatal aperture size in sugarcane plant leaves under drought to reduce water loss. Further Si application has enhanced stomatal density and aperture size under drought stress.
Smaller stomata can reduce the total leaf pore area, and smaller cells permit faster aperture response (Franks and Beerling 2009; Drake et al. 2013; Lawson and Blatt 2014). The more rapid stomatal response has shown maximum Water Use Efficiency (WUE) under fluctuating light conditions than prolonged water stress (Drake et al. 2013; McAusland et al. 2016; Kardiman and Ræbild 2018). Along with the stomatal size, the shape of guard cells and subsidiary cells are also proposed to affect stomatal functioning for water use efficiency and drought tolerance (Lawson and Vialet-Chabrand 2019).
Any stomatal damage affects carbon uptake, leading to the loss of photosynthetic machinery and reduced crop yield. Several authors have reported an increase in stomatal density and a decrease in size as an adaptive character during drought stress (Nawazish et al. 2006; Taratima et al. 2019). Few authors have also reported anatomical features such as more veins and lesser stomata per unit area in leaf to be closely related with sugarcane drought resistance (Mo and Zhou 1984; Meneses Rodriguez 1985; Malik 1986; Xu 1986).
6.4 Enlargement of Bulliform and Epidermal Cells
Bulliform cells are the water-storing epidermal cells present in the upper surface of leaves and play an essential role in regulating the rate of transpiration. Under moisture stress, bulliform cells assist in leaf rolling to avoid water loss through transpiration. Leaf rolling and reduced transpiration are related to plants’ drought resistance (Baranova 1987). The inefficiency of bulliform cells in leaf rolling and reduction in bulliform cell area under drought is considered as a susceptible character in sugarcane (Zhang et al. 2015; Taratima et al. 2019). With the water loss from the leaf, the perimeter/area ratio in bulliform cells is reported to reduce under drought. It is also noticed that the smaller ratio of perimeter and area is better for material and energy conversion (Wang et al. 2009; Zhang et al. 2015; Taratima et al. 2019).
Other important anatomical modifications reported in sugarcane under drought stress are enlargement of bulliform cells and epidermal cells, widened vesicles in bulliform cells, and bulliform cells with thin cell walls (Nawazish et al. 2006; Taratima et al. 2019). Under drought stress conditions, the pit of sclerenchyma cell walls is also reported to increase (Bosabalidis and Kofidis 2002).
6.5 Thickening of Leaf Lamina and Cuticle Layer
In sugarcane, the thickening of adaxial and abaxial cuticles covering the epidermis happens under both drought and salinity (Mo and Zhou 1984; Taratima et al. 2019). Along with the cuticle layer, increased lignification of cells around the vascular bundle is found in drought-resistant sugarcane varieties (Zhu et al. 2010). Strong lignification around the vascular bundle protects the conducting tissues under drought stress.
6.6 Other Anatomical Features
The size of bundle-sheath cells and vascular bundles gets modified under drought stress in sugarcane (Wu et al. 2011). Under moisture, increase in the vascular bundle size improves water and food transportation efficiency (Bosabalidis and Kofidis 2002). The number of vessels per unit area in sugarcane roots and stems is positively correlated with drought resistance (Tan 1988). Under severe drought stress, plasmolysis of chloroplasts is reported in sugarcane (Zhang et al. 2015). Movement of chloroplasts towards the center of the cell, change in shape, and increase in starch content are shown in susceptible sugarcane genotypes (Zhang et al. 2015). Reduced length, width, and width/length of chloroplasts are effective indexes for drought and salinity (Wu et al. 2011).
6.7 Root Anatomical Traits
Roots are the organs to detect moisture stress, and the physiological and molecular signals to induce resistance are sent by the roots (Atkinson and Urwin 2012). These root system signals help the plant adapt through various biological mechanisms to maintain optimal growth and yield under stress conditions (Sieburth and Lee 2010). Roots not only initiate the molecular signaling, but also modify the root architecture and anatomical traits, which contributes to enhance above-ground performance. Root System Architecture (RSA) plays a vital role in the agronomic performance of a crop. The adaptive plasticity in root anatomical helps to maintain photosynthesis and stomatal regulation, resulting in better yield under stress conditions (Chimungu et al. 2014a, b, 2015; Kadam et al. 2015).
In sugarcane, the relationship between root and shoot growth under diverse conditions has shown a positive correlation, and the efficient root traits also determine to stalk dry weight (Glover 1967; Smith et al. 1999; Ferreira et al. 2017). Sugarcane root system is highly divergent, comprising of highly branched sett roots (roots originating from the sett), shoot roots (main roots originating directly from the shoot), and deep rope roots formed by the agglomeration of shoot roots (Lynch 2013; Valarmathi et al. 2020). Sett roots arise from root eyes of setts within 24 h after planting that are required essentially for settling development and eventually degrades after 30–40 days. Shoot roots are stable, thicker, and fleshier permanent roots that provide strong anchorage developed from shoot bases 5–7 days after planting. These roots penetrate deeper soil beyond 1.5 m providing access to deep soil water reserves. The development of these root types strongly contributes to the performance of the above-ground parts (Gregory 2006). In sugarcane, extensive root systems support physiological and morphological traits of the above-ground parts under early drought stress (Khonghintaisong et al. 2018; Smith et al. 2005). Among the Root System Architecture (RSA), deep rooting is an extensively studied and reported root trait under stress conditions. Tolerant sugarcane genotypes have a long root system compared to susceptible genotypes under both drought and salinity stress conditions (Kumar et al. 2017; Khonghintaisong et al. 2018; Ogbaga et al. 2020). The genotypes with deep and extensive root systems are selected as water stress-tolerant genotypes (Smith et al. 2005). Long roots result in better water uptake, a desirable trait to extract deep soil moisture when water is limiting (Tardieu et al. 1992; Blum 2005; Tardieu 2012). At the cellular level, increased biosynthesis of lignin has one of the most crucial reactions under water-limiting conditions. The increased biosynthesis of lignin leads to cell-wall thickening of the vascular tissues, endodermis, and exodermis (Enstone et al. 2002; Naseer et al. 2012).
Anatomically monocot roots are characterized by the presence of two highly suberized layers called endodermis and pericycle. These two cell layers play a significant role in selective absorption as well as mineral and water uptake (Vásquez 2003). The pericycle is the meristematic layer, the source of lateral roots and surrounds the vascular bundle or stele (Richards and Passioura 1981). The major challenge for the plant under moisture stress is to protect the root water-conducting tissues from hydraulic pressure. Another challenge is to protect the meristematic layer pericycle for the growth of lateral roots. These two modifications are achieved either by lignifying the cells surrounding the vascular cylinder or by reducing the diameter of the xylem vessels. Only three authors have so far worked on the anatomical structures of sugarcane roots under drought conditions (Queiroz-Voltan et al. 1998; Chaves et al. 2009; da Cruz Maciel et al. 2015). The anatomical features studied in sugarcane are described in detail in separate sections.
6.8 Reduced Xylem Diameter
It is reported that continuous drought intensifies the imbalance between water transport and transpiration (through stomata and cuticles). This imbalance develops highly negative water potential and increases xylem tension, leading to bubble formation or cavitation of the vessel elements. Cavitation interrupts the flow through the xylem elements and may reduce the stomatal conductance, rate of photosynthesis, and, consequently, growth (Tyree and Sperry 1989). Under moisture stress conditions, this is the first symptom that directly affects the hydraulic system. To avoid this problem, the major adaptive root plasticity in the root system is making the hydraulic system more resistant and preventing cavitation (Kadam et al. 2015). Studies have demonstrated that the adaptive plasticity of xylem elements is the key to improve water use efficiency. The efficiency of the xylem hydraulic conductance shows direct relation to drought resistance and sustained yield. Reduced metaxylem diameter is very common in plants under water stress, and reductions in diameter of the metaxylem elements result in greater resistance to water flow (Passioura 1982; Melo et al. 2007). The tolerant sugarcane genotype RB867515 showed reduced vessel diameter under drought conditions (da Cruz Maciel et al. 2015). Several studies have also reported early stomatal closure as an adaptive mechanism that prevents xylem cavitation (Tardieu and Davies 1993; Plaut et al. 2012). Two major anatomical root traits have been reported to increase hydraulic root resistance: reduced xylem diameter and increased xylem number (Richards and Passioura 1981; Plaut et al. 2012).
6.9 Increased Exodermal Layer
Exodermis is the unicellular cell layer below the outermost epidermal layer in roots. Both epidermis and exodermis serve as apoplasmic barriers to transport water and ions to the inner vascular cylinder (Enstone et al. 2002; Enstone and Peterson 2005). The increased exodermal layer acts as a barrier for oxygen and water movement (Colmer 2003). On the other hand, a thin exodermis allows free radical oxygen and water movement. The rhizosphere, with better-aerated conditions, protects the roots against phytotoxins (Armstrong et al. 2000; Soukup et al. 2002). The low oxygen levels also stimulate ethylene synthesis, which inhibits root elongation. da Cruz Maciel et al. (2015) showed that roots of susceptible sugarcane genotypes had the highest number of exodermis.
6.10 Thin-Walled Exodermis
The deposition of suberin in the cell wall of the exodermis makes the layer thicker. The suberin layer acts as a barrier and prevents the radial loss of oxygen to the rhizosphere. In contrast, the barrier increases the longitudinal diffusion of oxygen in the aerenchyma (Soukup et al. 2002). Similar to the condition in increased exodermal layer, a thick-walled exodermis reduces the aeration in roots. It is also shown that the suberized exodermis reduces the flow of water and minerals from epidermis to cortex and the vascular cylinder (Prado 2005). A drought-tolerant sugarcane genotype RB867515 with thin-walled exodermis has been shown to facilitate water movement and maintain productivity under reduced moisture (Prado 2005; Ferreira et al. 2007; da Cruz Maciel et al. 2015).
6.11 Reduced Cortical Layer
The cell layer forms the cortex in between the exodermis and the stele. The reduced cortical layer is an adaptive trait in roots under drought conditions. It has been shown in several crops that reduced cortical cell layer reduces the metabolic costs of root growth and maintenance. Reduction in the cortical layer reduces the root volume, which has more metabolic demand than the stele region (Lynch 2013; Chimungu et al. 2014a, b). Reduced root volume decreases the metabolic demand under resource-limiting conditions. The drought tolerance is improved by reducing the metabolism cost, enabling continuous root growth and deeper soil exploration. Deeper soil exploration gives better water acquisition from the deeper soil reserves for better yield under water stress (Chimungu et al. 2014a, b; da Cruz Maciel et al. 2015).
6.12 Cortical Lysigenous Aerenchyma
The phytohormone ethylene triggers the formation of lysigenous aerenchyma in plants subjected to abiotic stress conditions (Bouranis et al. 2007). Aerenchyma develops intercellular spaces in the cortical layer. The reduced cortical layer filled with aerenchyma is found to be an adaptive character under drought as well as waterlogging conditions. The presence of aerenchyma is reported to have two important roles under drought conditions such as (1) it prevents the sudden shrinking of cortical cells due to the change in hydric potential and (2) the air spaces in the aerenchyma layer help in avoiding excess loss of water from the compact cortical layer (Melo et al. 2007). Aerenchyma cells facilitate better O2 diffusion, which helps to maintain aerobic respiration and cellular metabolism in roots (Vasellati et al. 2001; Bouranis et al. 2007; Melo et al. 2007). The presence of aerenchyma in the roots of sugarcane genotypes tolerant to drought has been reported (da Cruz Maciel et al. 2015).
6.13 Endodermis with U-Thickening
The endodermis is the outermost safety layer surrounding the stele and functions as an apoplasmic layer in regulating the movement of water, ions, and hormones into and out of the vascular system. In sugarcane under drought conditions, the anticlinal and inner periclinal walls of endodermal layers were found to be thickened (da Cruz Maciel et al. 2015). This is called U-thickening, which is more in the tolerant genotype than the susceptible sugarcane genotypes (da Cruz Maciel et al. 2015; Valarmathi unpublished data). Endodermal thickening is reported to play an important role in the conduction of water and photosynthates under both salinity and drought stress conditions. The thickening of endodermal cells helps to protect the vascular cylinder from damage due to hydraulic resistance and also prevents excess water loss from the stele region. Increased lignification of root endodermal cell wall is found to be one of the major salinity tolerance strategies in the roots of halophytes (Barzegargolchini et al. 2017).
6.14 Sclerification of Pericycle
As already mentioned, the pericycle is the meristematic layer, which is the source of lateral roots and surrounds the vascular bundle or stele (Richards and Passioura 1981). A common feature of the roots of monocots is the sclerification of the pericycle under drought and salinity stress (da Cruz Maciel et al. 2015). The sclerification of the pericycle helps to protect the vascular cylinder and increases the hydraulic resistance, while it reduces the morphogenic ability of this layer to form lateral roots (Ferri et al. 2000; Raven et al. 2008). In sugarcane, sclerified pericycle is reported intolerant genotypes under drought conditions (da Cruz Maciel et al. 2015). Sclerification of pericycle may prevent the cellular damage during stress, once the cessation of stress if the pericycle is intact, new roots will arise.
6.15 Conclusion
Sugarcane is an economically important crop for sugar and bioenergy production. Abiotic stress factors such as drought, salinity, high temperature, and waterlogging impact sugarcane productivity. Drought and salinity stresses are considered as one of the most deleterious stresses affecting sugarcane yield losses. Developing a tolerant genotype is essential to sustain sugarcane production under extreme environmental conditions. Studying the physiological, anatomical, and molecular changes during stress is essential to develop a tolerant genotype with a holistic approach. Very limited studies have been carried out to understand the anatomical tolerance mechanisms in sugarcane. However, the details given in this chapter show that anatomical feature of sugarcane leaf and root responds to stress conditions, and they also help in imparting tolerance to sugarcane crops. These traits can be used as a marker trait to identify the most stress-resistant genotype.
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Valarmathi, R., Mahadeva Swamy, H.K., Appunu, C., Kambale, R., Sudhagar, R. (2022). Anatomy of Tolerance Mechanisms in Sugarcane Crop to Abiotic Stresses. In: Verma, K.K., Song, XP., Rajput, V.D., Solomon, S., Li, YR., Rao, G.P. (eds) Agro-industrial Perspectives on Sugarcane Production under Environmental Stress. Springer, Singapore. https://doi.org/10.1007/978-981-19-3955-6_6
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