Abstract
Environmental stresses have major impacts on the morphological, physiological, and biochemical processes of plants. Among these stresses, drought is the major one which greatly restricts crop productivity globally. When challenged by drought, plants promote the expression of ABA biosynthesis genes which results in ABA accumulation. Increase in ABA level promotes stomatal closure to increase plant’s adaptative response to drought stress. To handle and restrain the negative impact of drought stress, it is important to understand how plants respond to drought and the involvement of ABA in plant adaptation to drought stress at a molecular level. Under drought stress, ABA biosynthesis is the most significant event to protect plants from the dehydration stress. ABA biosynthesis is a complicated process that is mainly regulated by ABA biosynthetic enzymes. This review highlights the recent advancements in ABA biosynthesis and its involvement in plant adaptation to drought stress to improve their growth and development under water-deficient conditions.
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Introduction
Being sessile by nature, plants face several challenges that alter their growth and development (Zhu 2016). These challenges are known as stresses and trigger several changes such as gene expression, growth retardation, and cellular metabolism, which can reduce overall yields. Very few plant species show tolerance to a given stress in a time-dependent manner after being exposed to it (Oh et al. 2014; Verma et al. 2013). Environmental stresses are categorized into two classes: biotic and abiotic. Biotic stress occurs when plants are exposed to biological factors that affect their growth and development, such as pathogen and insect attacks. In contrast, abiotic stresses are imposed on plants by chemical or physical factors in the environment, such as drought, salinity, and temperature (Verma et al. 2013; Chen et al. 2021). Such stresses represent the main causes of crop failures worldwide, reducing crop productivity and the average yields of economically important crops by amounts that may be life-threatening (Bray et al. 2000; Huang et al. 2008). Severe stress can lead to the death of a plant by restricting flowering and seed formation and promoting senescence (Verma et al. 2013). Thus, environmental stresses have been one of the most fascinating areas of research for plant scientists over the past 20 years.
Understanding how plants deal with these stresses and how they sense, transduce, and react to environmental stimuli has been given significant attention in the last two decades (Swain et al. 2023). Signal transduction provides strong support for different stress responses in plants on multiple levels (Markham and Greenham 2021). For instance, salinity and drought stresses induce osmotic stress, which promotes the accumulation of secondary metabolites to control ion toxicity, plasma membrane disruption, reactive oxygen species (ROS) accumulation, and cell wall disorder (Praveen et al. 2023). Plants respond to abiotic stresses most commonly through signal transduction, which in turn reacts to DNA methylation (Yu et al. 2024). Following that, RNA transcription occurs, which further leads to protein translation (Alberts et al. 2022). Next, it produces fresh and new proteins that promote an adaptative response to abiotic stress (Fig. 1).
Plant adaptive responses to abiotic stresses. A representative diagram highlighting the responses of plants to abiotic stress at the molecular level starting from signal transduction
A typical signal transduction pathway begins with signal perception, followed by the generation of secondary messengers such as calcium, inositol phosphates, and ROS. Finally, it modulates the intracellular calcium level in the cytosol, which is sensed by calcium-binding proteins called Ca2+ sensors. These sensors tend to be free of any enzymatic activity and exhibit structural modifications that are Ca2+-dependent (Ryder et al. 2023). These sensors interact with their potential partners to initiate a phosphorylation cascade and regulate transcription factors or stress-responsive transcription mediators, which regulate the expression of target genes (Guan et al. 2013; Chen et al. 2021; Wu et al. 2022). The end products of these stress-responsive genes promote plant adaptation to the initiating stress (Mahajan and Tuteja 2005) (Fig. 1). This highlights the fact that the adaptation of a plant to stress is a completely mechanistic package that includes several metabolic processes, signaling cascades, and gene expression (Dong et al. 2015; Chen et al. 2021).
Plant Response to Drought Stress
Drought stress is a major environmental stimulus and has a significant impact on global crop security (Chieb and Gachomo 2023). Water constitutes 80–95% of the body of a plant as fresh biomass, which plays important roles in several physiological processes (Abbasi and Abbasi 2010; Brodersen et al. 2019). Consequently, scientists firmly believe that drought is the single biggest threat to future worldwide agricultural production, especially for crops cultivated in vulnerable areas (O’Connell 2017; Diatta et al. 2020). Irregularity in the rainfall distribution, evapotranspiration, and water-holding ability of the rhizosphere are the major factors that contribute to the unpredictable nature of drought. There are also times when plants are unable to obtain water from the soil despite a sufficient amount of moisture in the root zone, a phenomenon called physiological drought (Daryanto et al. 2017).
There are several factors that significantly affect the response of a plant to drought stress, including the growth stage, species, drought severity, and timing (Gray and Brady 2016). Therefore, the ability to withstand the effects of stress and adapt their growth capabilities varies among plant species (Osakabe et al. 2014; Bielach et al. 2017). At the molecular level, the responses of plants to drought stress are improved by several mechanisms, including those involved in signal transduction (Kaur and Asthir 2017; Zandalinas et al. 2020). To tolerate a water-deficit condition, plants promote ion transportation and modulate the activity of transcription factors, as well as ABA biosynthesis and stomatal movement (Prakash et al. 2019). Under drought stress, the transpiration rate from the leaves reduces the water-uptake efficiency of the roots (Goche et al. 2020). The adaptation of a plant to drought mainly involves closing its stomatal aperture to reduce water loss and expanding its roots to absorb more water from the soil (Martínez-Vilalta and Garcia‐Forner 2017).
Drought stress affects plants in various physiological, biochemical, morphological, and ecological ways (Ortiz et al. 2015). The physiological aspects include the promotion of stomatal closure, a reduced photosynthesis efficiency, enhanced oxidative stress, changes in the cell-wall integrity, a reduced transpiration rate, an increase in its internal body temperature, a reduced CO2 level, and proline accumulation (Hu et al. 2022). The biochemical aspects include decreases in the Rubisco and photochemical efficiencies, the promotion of ROS production, changes in the cell-wall integrity, decreases in its growth ability and water transpiration, an increase in its body temperature, reduced CO2, the cessation of assimilation, and the accumulation of proline contents. The morphological aspects include drought escape (DE), dwarfness, reduced leaf size, the promotion of leaf rolling, changes in the stomata position and leaf color, reduced leaf longevity, permanent leaf wilting, and changes in the leaf angle (Riboni et al. 2013, 2016; Corso et al. 2020; Fig. 2). To mitigate the effects of drought, plants depend on the previous occurrence of drought, drought intensity, and existence of other stresses (Thomason and Battaglia 2020).
Representative chart for drought stress effect on plants. This representative chart illustrates the drought stress impacts on plants, including physiological, biochemical, and morphological events
Drought Stress and Accumulation of ABA
Phytohormones play crucial roles in plant growth and development and stress responses (Sah et al. 2016; Ali et al. 2024). Drought stress is a well-known cause of the accumulation of several phytohormones that promote adaptive responses in plants (Ismail et al. 2018). These accumulated phytohormones enhance several physiological and developmental processes, such as the osmotic balance, negative phototropism in roots, and stomatal closing (Lim et al. 2015). Among the phytohormones, ABA plays a central role in drought stress responses (De Ollas et al. 2013). The drought-induced accumulation of ABA improves the resilience of a plant to drought stress (Ng et al. 2014). In addition to drought tolerance, ABA is important for the growth and development of plants under non-stress conditions (Lee et al. 2006). ABA also promotes and maintains seed dormancy (Rodríguez-Gacio et al. 2009). Furthermore, ABA alters the root structure and architecture, which changes the growth pattern in plants (Puértolas et al. 2015). ABA also induces leaf senescence, as evidenced by the late-senescence phenotypes of several ABA-deficient mutants (Yang et al. 2003; Passioura 2006). Under non-stress conditions, ABA and elevated CO2 levels enhance partial or complete stomatal closure (Kim et al. 2010). When elevated by drought, ABA promotes stomatal closure, which reduces the water loss from leaves (Hasan et al. 2021). The ABA accumulated as a result of drought regulates the expression of several genes, particularly drought-responsive genes, which play key roles in the drought tolerance of a plant (Fujita et al. 2011). Several transcriptomic studies have shown that 50% of ABA-regulated genes are governed by drought stress. Among these, 245 genes have already been identified in Arabidopsis (Seki et al. 2002). Like Arabidopsis, 43 out of 73 stress-responsive genes in rice have been reported to be regulated by ABA and drought stress (Rabbani et al. 2003). Together, these reports suggest that drought-induced ABA accumulation plays an important role in the response of plants to drought stress, specifically by promoting stomatal closure to prevent water loss from leaves.
Role of ABA Biosynthesis Enzymes in Drought Stress
Drought-induced ABA synthesis is a critical process that supports the adaptive responses of plants during drought stress. Previous studies have shown that the phytohormones accumulated as a result of drought promote adaptation responses via several signal transduction mechanisms (Bharath et al. 2021). A drought stress-activated ABA biosynthesis pathway was proposed by Xiong and Zhu (2003). This process involves redox signals, Ca+ 2 signaling, phosphoprotein cascades, and transcription factors that activate the expression of ABA biosynthetic genes (Xiong and Zhu 2003). ABA biosynthesis is a ubiquitous C15 isoprenoid process during drought stress, which is well characterized through forward genetic screening and several other enzymatic steps that have been identified in different plant species (Marin et al. 1996; Tan et al. 1997; Burbidge et al. 1999; Agrawal et al. 2001; Xiong and Zhu 2003; Dong et al. 2015; Liu et al. 2020).
The ABA biosynthesis process begins in plastids with the precursor carotenoid zeaxanthin. This is first repeatedly epoxidized into violaxanthin by zeaxanthin epoxidase (ZEP), which is also known as ABA deficient1 (ABA1) (Koornneef et al. 1982; Bouvier et al. 1996). Violaxanthin is then converted into neoxanthin by ABA4 (North et al. 2007). An unidentified isomerase then isomerizes both violaxanthin and neoxanthin at the C9–C10 (C9′–C10′) double bond, resulting in the production of 9-cis-violaxanthin and 9′-cis-neoxanthin (Dong et al. 2015). The 9-CIS-epoxycarotenoid dioxygenases (NCEDs) enzymes cleave these 9(′)-cis-epoxycarotenoids at the C11–C12 (C11′–C12′) double bond, producing a C25 apocarotenoid and the ABA precursor xanthoxin (C15) (Schwartz et al. 1997; Qin and Zeevaart 1999; Tan et al. 2003; Dong et al. 2015). This cleavage reaction is known as the rate-limiting step in the ABA biosynthesis pathway. Then, ABA2/3 and ABSCISIC aldehyde oxidase 3 (AAO3) enzymes convert xanthoxin into ABA after being translocated from plastids to the cytoplasm (Seo et al. 2000; González-Guzmán et al. 2002; Dong et al. 2015; Fig. 3). ABA2 is a cytosolic short-chain reductase that converts xanthoxin into abscisic aldehyde (González-Guzmán et al. 2002), and AAO3 is an aldehyde oxidase that mediates the oxidation of abscisic aldehyde into ABA (Seo et al. 2000; Dong et al. 2015), while ABA3 is a molybdenum cofactor sulfurase that provides enzymatic activity to AAO3 (Xiong et al. 2001).
Schematic representation of ABA biosynthesis pathway. Illustration of ABA biosynthesis pathway with different events. The first step occurs in the plastid, and the last step occurs in the cytosol. In the plastid, ZEP and NCED genes play essential roles in the synthesis into cytosol, whereas SDR and AAO are very important to the synthesis of ABA in the cytosol
Generally, drought stress enhances the expression of genes coding for ABA biosynthetic enzymes to accumulate endogenous ABA such as ZEAXANTHIN EPOXIDASE (ZEP/LOS6 [LOW EXPRESSION OF OSMOTIC STRESS-RESPONSIVE 6]/ABA1), the ALDEHYDE OXIDASE (AAO3), a 9-CIS-EPOXYCAROTENOID DIOXYGENASE (NCED3), and MOLYBDENUM COFACTOR SULFURASE genes (MCSU; also known as LOS5/ABA3) (Dar et al. 2017). However, some transcription factor families such as bZIP, MYB, MYC, NAC, ERF, and DREB/CBF also controlled their expression (Verma et al. 2016). In the ABA biosynthesis pathway, ZEP was the first identified gene, whose expression has been studied in all parts of the diverse plant species (Audran et al. 1998; Xiong et al. 2002). It was thought that ZEP does not limit ABA biosynthesis in photosynthetic tissues. Because the amount of 9-cis-epoxycarotenoid (precursor that occurs downstream of the ZEP-catalyzed reaction) is several times higher in photosynthetic tissues on a molar basis than ABA produced during stress. The transcript level of ZEP gene in the leaves of tobacco and tomato remains unchanged in drought, however, unexpectedly, it increases during the daytime (Audran et al. 1998; Thompson et al. 2000), which reflects circadian rhythm regulation. Unlike tobacco and tomato, the Arabidopsis ZEP gene shows basal transcript levels in non-stress condition, however, its expression level clearly increases in drought stress both in shoots and roots (Xiong et al. 2002). The transcriptomic studies with other ABA biosynthesis enzymes (such as ABAs, SDR, MCSU, AAO3, etc.) are less controversial. However, the cleavage step, particularly rate-limiting enzymes got huge attention in the last two decades. Drought stress rapidly increased the expression levels of NCEDs genes in tobacco (Tan et al. 1997), tomato (Burbidge et al. 1999), bean (Phaseolus vulgaris; (Qin and Zeevaart 1999), Arabidopsis (Iuchi et al. 2001), cowpea (Vigna unguiculata; (Iuchi et al. 2000), and avocado (Persea americana; (Chernys and Zeevaart 2000). The oversight of ABA biosynthesis is crucial for regulating ABA levels, adjusting plant stress responses, and developmental programs. Stress-inducible ABA biosynthesis genes may therefore be controlled by DRE/CRT class of stress-responsive genes (Xiong et al. 2002), because they contain both the DRE- and ABRE-like cis-elements in their promoters (Xiong et al. 2001; Bray, 2000). To better understand, research requires at molecular level of transcription factors with the cis-elements that activate the ABA biosynthesis genes. Indeed, several loci were found in over six different screening techniques, however, did not find a direct regulator of ABA biosynthesis. The correlative studies on sugar, ethylene, and ABA biosynthesis in growth and physiological processes (Ghassemian et al. 2000; Hansen and Grossmann 2000; González-Guzmán et al. 2002), indicates the possibility of some signaling components in other hormone response pathways. Like era3 (enhanced response to ABA 3) and ein2 (ethylene insensitive 2) could be two examples of this coregulation. The ZEP transcript level was higher in ein2, suggesting that enhanced ABA biosynthesis is likely the reason why era3/ein2 plants had a basal ABA level twice that of the wild type (Ghassemian et al. 2000). The clear effect of ein2 mutation on ABA biosynthesis may result from the intricate interaction between several hormonal pathways.
Alternative tests such as gas exchange (sensitivity to CO2) and guard cell regulation (Mustilli et al. 2002), may identify new loci that control ABA biosynthesis or signaling. Molecular genetic techniques, like the one employed in the screen for stress signal transduction mutants (Ishitani et al. 1997), may be more effective in identifying signal transduction components since gene expression is more responsive to stress regulation than some of the apparent phenotypes. This method involves transcriptionally fusing the promoters of stress-inducible ABA biosynthesis genes such as AtNCED3, AtMCSU, and AtAAO3 to a reporter gene. This allows for the isolation of mutants exhibiting changed reporter gene expressions in response to abiotic stresses. These tests could reveal new ABA biosynthesis regulating mechanisms (Xiong and Zhu 2003). With the full genome of Arabidopsis available and a wealth of expression data, reverse genetics techniques ought to make it easier to find novel regulatory elements in the signaling pathway that leads to the synthesis of ABA. Molecular biology, biochemistry, genetics, and genomics will all need to be combined to fully comprehend how ABA production is regulated.
Epigenetic Regulation of ABA Biosynthesis Genes in Drought Stress
The genetic manipulation of ABA biosynthesis is a very established process, however, in the recent past, several reports stated that epigenetic modification is also an integral part of the endogenous ABA regulation during drought stress (Chinnusamy et al. 2008; Baek et al. 2020; Khan et al. 2020; Gu et al. 2021). Several plant species have been reported to regulate drought stress epigenetically including histone acetylation and deacetylation (Li et al. 2021; Praveen et al. 2023), as well as the chromatin remodelers that regulate ABA biosynthesis genes via transcription activation and deactivation (Khan et al. 2020). The dynamic activity of histone acetyltransferases (HATs) and histone deacetylases (HDAs) in response to drought stress has been widely studied in drought resilience across different plant species (Baek et al. 2020; Khan et al. 2020; Zhang et al. 2020; Hou et al. 2021; Li et al. 2022). In Arabidopsis, the acetylation mark at lysine 9 (H3K9ac) acts as a major regulator of chromatin modification at the promoters of several drought-responsive genes to control their transcript abundance (Zheng et al. 2016). Dehydration increases the endogenous ABA level by promoting histone acetylation of ABA anabolism genes and reducing histone methylation of the ABA biosynthesis genes (Gu et al. 2021), indicating a correlation between epigenetic modification and ABA accumulation (Fig. 4). The HATs and HDAs dynamic activity also controls the ABA biosynthesis pathway, which is also the primary signaling pathway for drought stress in plants (Kumar et al. 2021; Li et al. 2021). In contrast to ABA biosynthesis, the ABA catabolic pathway also working in drought stress, as we previously reported that HDA9-PWR making a complex with ABI4 to regulate histone status of CYP707A1/2 (ABA catabolic enzyme) in drought tolerance (Baek et al. 2020; Khan et al. 2020), suggesting the importance of epigenetic regulations of ABA catabolic genes under drought stress.
Schematic representation chromatin remodeling in drought stress. Illustration of chromatin status in normal and drought condition. In normal conditions, the condensed status of chromatin does not promote the ABA level due to inactivation of ABA biosynthesis genes. Under drought stress, the active and open status of chromatin promotes the endogenous ABA level through the activation of ABA biosynthesis genes
Role of E3-ligases in ABA Biosynthesis
Previous studies have shown that a significant number of E3-ubiquitin ligases in plant genomes have been identified as regulators of phytohormone biosynthesis (Liu and Stone 2011). The Arabidopsis XERICO is an E3-ubiquitin ligase with a small RING-H2 domain, which regulates the endogenous ABA level and expression of the NCED3 gene in the drought-stress response (Ko et al. 2006). The senescence-associated E3 ubiquitin ligase 1 (SAUL1), which is also known as PLANT U-BOX 44 (PUB44), controls ABA production by enhancing the activity of the AAO3 enzyme to prevent premature senescence (Raab et al. 2009). Previously, we have shown that HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 15 (HOS15), a WD40 domain protein, is a multifunctional protein that regulates several physiological processes and stress responses in plants (Ali and Yun 2020). We have also shown that HOS15 is involved in freezing stress, drought stress, floral transition, plant immunity, leaf senescence, and miRNA biogenesis (Park et al. 2018, 2019; Ali et al. 2019; Shen et al. 2020; Zareen et al. 2022; Lim et al. 2023; Park et al. 2023). In addition, we have shown that HOS15 negatively regulates ABA signaling and drought stress by affecting OPEN STOMATA 1 (OST1) stability, which is a core component of the ABA signaling cascade (Ali et al. 2019). However, it is unclear how HOS15 interferes with ABA biosynthesis and whether HOS15-mediated drought stress responses involve ABA biosynthesis. Nonetheless, some indications suggest that HOS15 may be involved in the ABA biosynthesis pathway because HOS15 regulates the expression levels of ABA biosynthetic genes such as NCED2/3/5/6/9, and hos15-2 plants show higher ABA contents under dehydration stress (Ali et al. 2019). Further molecular studies are required to better understand how HOS15 regulates the ABA biosynthesis pathway.
Concluding Remarks
According to prior studies, the mechanism by which plants respond to drought stress is highly complicated, involving multiple single and complex components that help to control stress responses. The genetic disruption of several genes has been identified to contribute to the morphological phenotypes of plants as well as their stress responses. This review summarized the importance of ABA biosynthesis, which is crucial to the physiological, biochemical, and morphological functions of plants and improves their adaptability to water-deficient conditions. Drought stress primarily activates the ABA biosynthesis enzymes involved in ABA production to improve stomatal closure, which reduces the severe effects of drought stress on plants. Several ABA biosynthesis components have been reported, including AAO3, NCEDs, and ABA1/2/3/4. These have different molecular mechanisms that contribute significantly to the adaptative responses of plants to drought stress. The importance of the ABA biosynthesis pathway under drought stress is still an open debate among scientists and researchers, necessitating further investigation to acquire in-depth knowledge.
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Zareen, S., Ali, A. & Yun, DJ. Significance of ABA Biosynthesis in Plant Adaptation to Drought Stress. J. Plant Biol. 67, 175–184 (2024). https://doi.org/10.1007/s12374-024-09425-9
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DOI: https://doi.org/10.1007/s12374-024-09425-9