During its whole life cycle, a plant’s physical survival is threatened by exposure to various biotic and abiotic stresses, which can cause morphological and physiological changes that limit growth and productivity (Bajguz and Hayat, 2009). A thin and tough layer called the cell wall surrounds plant cells to provide structural strength and act as a protective barrier against both biotic and abiotic stresses, such as pathogen attack and salinity (osmotic stress) (Taiz and Zeiger, 1998).

Phytohormones are chemical mediators that enable plants to coordinate a variety of cellular processes such as rapid responses to external stimuli (Deb et al., 2016); regulation by phytohormones is required for cell wall sensing and reconstruction during adaptive responses to adverse conditions (Didi et al., 2015; Houston et al., 2016). Brassinosteroids (BR) are a family of plant steroid hormones that elicit cell expansion (Vriet et al., 2013). Plant cell expansion and differentiation are inherently accompanied by a series of dynamic changes in cell wall composition (Hofte, 2015). The BR signaling pathway is fine-tuned to determine cell wall loosening or stiffening to assure the appropriate cell wall properties under various environmental conditions (Voxeur and Hofte, 2016). Application of exogenous BR has been proven to enhance crop tolerance to unfavorable conditions (Sharma et al., 2013), and genetic manipulation of genes that control endogenous BR levels can promote crop tolerance and improve biomass yield under a wide arrange of abiotic stress conditions (Wu et al., 2008; Ahammed et al., 2015).

The grass family (the Poaceae), one of the largest flowering plant families, covers one fifth of the earth’s land (Fincher, 2009). Grasses, including rice, maize, wheat, switchgrass, ryegrass and related species, dominate the majority of human food, livestock feed, biofuel resource and lawn and ornamental use. Grass cell walls constitute a major portion of the plant biomass and present unique features compared with those of dicots (Vogel, 2008). Therefore, understanding hormonal regulation of grass cell wall construction under adverse conditions is important for future manipulation of food and biofuel crops under climate change. Recent reviews have suggested how BR signaling underlies how plant cell walls sense pathogens and operate an active defense against pathogen attack (Underwood, 2012; Bellincampi et al., 2014; Malinovsky et al., 2014). In this review, we focus on the mechanisms of cell wall remodeling in grasses under the control of BRs as a response to abiotic stresses.

Plant cell walls mainly consist of the polysaccharide polymers cellulose, hemicellulose and pectin, along with lignin and a small amount of structural protein (Bashline et al., 2014). Individual cellulose microfibrils are organized to form a highly ordered (crystalline) matrix via hydrogen bonds. Hemicellulose binds to the surface of cellulose to prevent cellulose microfibrils from clasping together. Pectin and structural proteins are embedded into the cellulose-hemicellulose network to enhance the correct assembly of cell wall components and, along with lignin, to provide additional mechanical strength (Taiz and Zeiger, 1998; Cosgrove and Jarvis, 2012).

There are two major types of cell wall according to composition and structure. Type I walls consist of a xyloglucan matrix into which cellulose microfibrils are embedded, with high levels of pectin and structural proteins and low levels of arabinoxylans, glucomannans, and galacto-glucomannans. In contrast, type II walls have a cross-linked network of glucuronoarabinoxylans bound to cellulose fibers, with various minor portions of pectin and structural proteins (Vogel, 2008). Type I cell walls are present in dicots, non-grass monocots and gymnosperms, and type II cell walls are present in grasses (Fincher, 2009). Additional notable features of grass cell walls include the presence of mixed-linkage β-glucans and the abundance of xylan and lignin deposited in secondary cell walls (Vogel, 2008). These unique aspects indicate the existence of genes specifically involved in grass cell wall biogenesis, many of which remain to be explored (Lin et al., 2016).

Among abiotic stresses, water-deficiency through drought, osmotic stress and salinity are the most challenging for crop growth and food production (Tenhaken, 2015; Feng et al., 2016). The water potential of the plant cell is in accordance with that of the environment surrounding the cell (Bray, 2007). Drought, osmotic stress and salinity decrease the water potential of the soil solution and water leaks from the cell to the external solution (Bray, 2007). As a consequence, this can lead to reduction of cell turgor and physical damage to the cell wall including disconnection of binding sites for wall components, loss of fragments from the wall, and decreased associations between the wall and the plasma membrane (Hamann, 2015b).

Another common reaction in plant responses to many stress conditions (such as heavy metal ions) is the generation of a burst of reactive oxygen species (ROS), which results in the toxicity of oxidative stress (Mittler, 2002). A rapid accumulation of ROS in plant cells inhibits the activity of antioxidants and antioxidative enzymes and can cause the degradation of lipids and even destruction of the cell membrane (Das and Roychoudhury, 2014). Moreover, the generation of OH by the Fenton reaction involving heavy metal ions or antioxidative enzymes is considered to cause plant cell wall loosening via breaking cross-linkages between ferulates and lignin (Karkonen and Kuchitsu, 2015).

A group of plasma membrane-localized receptor-like kinases (RLKs) and mechanosensitive ion channels (such as Ca²⁺ channels) are considered to directly or indirectly detect the impairment of cell wall integrity as a mechanical cue to sense adverse effects in the environment. They subsequently translate the physical changes in the cell surface to cellular signals (such as Ca²⁺ influx), which further trigger corresponding cascades of plant defense responses for stress management (Hamann and Denness, 2011; Feng et al., 2016). These responses are better understood in yeast than in plants (Hamann and Denness, 2011).

When perceiving environmental cues, plants translate them into physiological signals through coordination of the levels of phytohormones such as gibberellic acid (GA), abscisic acid (ABA), and BRs that will further trigger cellular responses to maintain integrity and remodeling of the cell wall (Ahammed et al., 2015). Recent findings have characterized the molecular machinery of BR signal reception and transduction in Arabidopsis (Wolf et al., 2012, 2014; Zhu et al., 2013). However, the BR signaling pathway in monocots still remains to be explored, although a few conserved components have been identified in rice (Yamamuro et al., 2000; Bai et al., 2007; Li et al., 2009; Tong et al., 2012; Vriet et al., 2013; Zhang et al., 2014; Zhang B. et al., 2016), maize (Zhang Y. et al., 2016) and Brachypodium distachyon (Feng et al., 2015). Here, we show a proposed model for the BR signaling pathway in grasses generally based on the information for rice (Figure 1). BR signaling is perceived by cells through its binding to the extracellular domain of a plasma membrane-bound receptor kinase, BRASSINOSTEROID INSENSITIVE 1 (OsBRI1) (Yamamuro et al., 2000; Zhu et al., 2013). BR-binding prevents BRI1 from associating with the negative regulator OsGSK and promotes BRI1 to interact with the co-receptor kinase BRI1-ASSOCIATED RECEPTOR KINASE1 (OsBAK1) (Li et al., 2009; Zhang et al., 2014). The trans-phosphorylation between OsBRI1 and OsBAK1 activates the kinase activity of BRI1, the intracellular domain of which initiates the signal transduction cascade within cells (Vriet et al., 2013). BR SIGNALING KINASE (BSK1) located in the cytoplasm is phosphorylated and activated by BRI1 leading to the activation of BRI1 SUPPRESSOR1 (BSU1) (Zhang B. et al., 2016). Through desphosphorylation, BSU1 negatively regulates OsGSK2, an inhibitor of the BRASSINAZOLE-RESISTANT1 (BZR) family of transcription factors (Tong et al., 2012). Upon BR signaling, OsBZR1 is activated by dephosphorylation and inhibition of its interaction with 14-3-3 proteins. This leads to a rapid accumulation of OsBZR1 in the nucleus to directly control the expression of BR target genes (Bai et al., 2007). In Arabidopsis, the BR-activated transcription factor BZR1 and its homologous gene BZR2/BES1 have been shown to directly bind to promoter regions of a large number of cell wall-related genes (Jiang et al., 2015), including the majority of cellulose synthase genes (Xie et al., 2011), and NAC and MYB transcription factors associated with regulatory pathways for lignin synthesis (Zhao and Dixon, 2011; Benatti et al., 2012). Though direct evidence is absent, grasses may operate a similar BR-mediated signal cascade to regulate the expression of genes involved in cell wall biogenesis.

Recent evidence suggests the association of BR signaling pathways with cell wall remodeling. Here, we discuss effects of BRs on cell wall loosening proteins and major structural cell wall components including cellulose, lignin and pectin, according to recent advances in both grasses and dicots.

The possible roles of BR signaling that contribute to cell wall remodeling are summarized in Figure 1. Few BR response targets have been established and much remains to be discovered about how BRs regulate the expression of cell wall related genes and corresponding enzymatic activity in grasses. In addition, the crosstalk between BRs and other phytohomones in controlling cell wall integrity is another area that requires more investigation (Bai et al., 2012; Huang et al., 2015; Deb et al., 2016). A better understanding of BR-mediated cell wall homeostasis will guide the design of genetic modification strategies to improve biomass and stress tolerance in grasses.

XR collected data from literature and wrote the manuscript. RD revised the article.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.