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Review

Crop Lodging and The Roles of Lignin, Cellulose, and Hemicellulose in Lodging Resistance

by
Qing Li
1,2,3,
Canfang Fu
1,2,3,
Chengliang Liang
4,
Xiangjiang Ni
4,
Xuanhua Zhao
1,2,3,
Meng Chen
1,2,3 and
Lijun Ou
1,2,3,*
1
College of Horticulture, Hunan Agricultural University, Changsha 410128, China
2
ERC for Germplasm Innovation and New Variety Breeding of Horticultural Crops, Changsha 410128, China
3
Key Laboratory for Evaluation and Utilization of Gene Resources of Horticultural Crops (Vegetables, Tea, etc.), Ministry of Agriculture and Rural Affairs of China, Changsha 410128, China
4
Vegetable Research Institute, Hunan Academy of Agricultural Science, Changsha 410125, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(8), 1795; https://doi.org/10.3390/agronomy12081795
Submission received: 14 May 2022 / Revised: 22 July 2022 / Accepted: 25 July 2022 / Published: 29 July 2022
(This article belongs to the Special Issue Recent Advances in Horticultural Crops-from Omics to Biotechnology)
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Abstract

:
With increasingly frequent extreme weather events, lodging has become an important limiting factor for crop yield and quality and for mechanical harvesting. Lodging resistance is a precondition for “super high yield” crops, and the question of how to achieve lodging resistance to guarantee high yield is an urgent scientific problem. Here, we summarize the anatomical results of lodging resistance stems and find that the lodging resistance of stems is closely related to stem components. Therefore, we focus on the roles of lignin, cellulose and hemicellulose, which provide stem rigidity and strength, in crop lodging resistance. By combing the synthetic regulatory molecular network of lignin, cellulose and hemicellulose, we find that only some of the genes involved in the biosynthesis and regulation of lignin, cellulose, and hemicellulose have been shown to significantly affect lodging resistance. However, many relevant genes remain to be studied in sufficient detail to determine whether they can be applied in breeding for lodging resistance. This work provides valuable information for future studies of lodging resistance.

1. Introduction

Lodging is a crucial issue in crop production because it not only reduces crop yield and quality but also increases the difficulty and cost of harvesting. Rajkumara [1] describes types of lodging as stem lodging and root lodging. Most studies report that stem lodging often poses a greater threat to crop production than root lodging [2,3]. Stem lodging can decrease the grain yield of maize by 5–43% [4]; in rapeseed, stem lodging can decrease yield by 10–30% (or >50% in severe cases), and the oil content also decreases by 10–30% [5]. There is a constant risk of lodging during the fruit setting stage of the peppers, which can lead to decreased yield and quality. In addition, lodging leads to increases in labor and production costs. In summary, lodging is an important limiting factor for crop yield, quality and mechanical harvesting.
Stem lodging resistance is a critical agronomic trait for crops. Morphological and physiological characteristics of a stem are closely related to lodging resistance. The plant stem not only provides rigidity and strength for the plant, but also ensures the transport of water and nutrients [6]. The mechanical strength and stiffness of the stem are key breeding indicators for resistance to stem lodging [7]. An increase in stem strength can enhance the maximum total stress that the stem can bear [8]. An increase in stem stiffness can enhance the resistance of stems to deformation [7]. It has been reported that the lodging resistance of stems is positively correlated with stem strength in maize, wheat, soybean and oat [9,10,11,12,13]. In addition, excellent stiffness lines can be recommended to plant breeders to select cultivars with strong lodging resistance in maize and oat [14,15]. Stem lodging is regulated by both environmental and genetic factors. However, environmental factors (wind, rain, temperature) are largely out of human control [16,17,18] in nature. Therefore, the genetic improvement of stem developmental processes through molecular means is an effective strategy to enhance lodging resistance [19,20]. Lodging resistance in crop plants is advantageous for high yield, high quality and lower production costs. Therefore, the ability to support crops with sufficient stem stiffness and strength is key to the successful commercial production of high-yield varieties. The mechanical properties of plant lodging resistance are affected by many factors (such as plant height, crown width, stem diameter, and stem components) [7]. Here, we discuss only the roles of lignin, cellulose and hemicellulose.
Lignin, cellulose, and hemicellulose, as the most abundant structural carbohydrates in plants, play important roles in crop lodging resistance [21,22,23,24]. They are the main components of the cell wall and secondary cell wall [25]. They can improve the mechanical strength and rigidity of the stem and maintain the stability of cell wall components [26,27,28]. This review systematically analyzes the causes of crop stem lodging. We summarize the anatomical results of stem lodging resistance and find that the lodging resistance of stems is closely related to stem components. Therefore, we focus on the roles of lignin, cellulose and hemicellulose, which provide stem rigidity and strength, in crop lodging resistance. By combing the synthetic regulatory molecular network of lignin, cellulose and hemicellulose, we find many genes involved in the synthesis and regulation of lignin, cellulose, and hemicellulose, and infer that these genes contribute to lodging resistance. In addition, we believe that the influence of cultivation practices on these three structural carbohydrates cannot be ignored. Therefore, we believe that the interaction between environmental factors and the genetic factors of crop lodging resistance, such as lignin, cellulose and hemicellulose, is worthy of further study. Our work provides valuable information for future study into lodging resistance.

2. Crop Stem Characteristics and Lodging

2.1. Environmental Factors Affecting Stem Lodging

Lodging in crops is influenced by many environmental factors [29,30], such as wind, rain, radiation, and temperature [17,29,31,32,33,34] (Figure 1). Wind-induced force on the upper section of a shoot or plant results in a bending moment at the plant base. If the bending moment exceeds the strength of the stem base, stem lodging is expected to occur [2,35,36]. Generally, lodging occurs when the weight of the upper part of a plant increases due to the interception of rainfall [37]. Lodging is often severe when the lower stem parts are weakened by disease or the over-application of nitrogenous fertilizer [38,39,40,41,42]. Severe lodging also occurs when the shearing cohesive bond strength of the soil particles around the root system are greatly deteriorated by rainfall (i.e., anchorage failure) [43]. Light is a decisive factor for internode elongation, whereas shade results in stem elongation, reduced dry matter accumulation, and lodging [44]. Studies have shown that soybeans can avoid shade to reduce lodging [45]. High temperature significantly reduces root lodging resistance, as indicated by a dramatic reduction in root anchorage and in factors protecting against anchorage failure [46]. In contrast, low temperature and high radiation are beneficial for dry matter accumulation and increase the mechanical strength of corn straw [34].

2.2. Agronomic Practices Affecting Stem Lodging

In agricultural production, stem lodging is influenced by agronomic practices. The soil environment, sowing date, sowing density, fertilization application status, planting method, and incidence of pests and diseases can greatly affect the degree of crop lodging [9,47,48,49,50]. Physical and chemical properties of soil are closely related to the anchoring ability of plants; the texture, hardness, porosity, and nutrients in the soil directly affect root development in plants, which in turn affects lodging resistance [51,52,53]. Bian et al. [54] have reported that rotary tillage before seeding and direct seeding into stubble would be suitable practices to reduce lodging for maize production. The effect of sowing date on crop lodging resistance should not be ignored. In wheat, delayed sowing, even by as little as a week, can reduce lodging by up to 49.6% [55]. Reduced planting density also causes a great reduction in lodging risk [56,57,58,59,60,61]. Low-density planting has been shown to increase mechanical strength, lignin accumulation, stem diameter, and lodging resistance by improving crop canopy structure [27,62,63]. However, under high-density planting conditions, low dry matter remobilization has been shown to be beneficial for stem strengthening and reducing the risk of stem lodging [64]. In another study, the risk of lodging increased with increasing N rates [65,66]. High N treatments rapidly decreased lignin deposition in the sclerenchyma cells of mechanical tissues and in the large and small vascular bundles [67,68]. Controlled nitrogen application increased lodging resistance, the uptake of potassium (K) and silicon (Si), delayed stalk senescence under drought conditions, improved stalk strength, and influenced stalk composition in the later growth stages [69,70]. Si is associated with the sturdiness and rigidity of plants [71]. The practical application of silicon fertilizer increased root diameter, stem SiO2 content, and fracture strength, and decreased plant height and lodging [72,73,74]. K application significantly increased the breaking strength of rice by 40.94–144.24%, and decreased lodging by 13.14–36.72% [75,76]. Reasonable fertilization measures can, therefore, ensure high yield and lodging resistance [77,78]. Stalk rot, sheath blight, Mexican rice borer (Lepidoptera: Crambidae), and charcoal rot all damage the plant stem. This weakens the phloem and conduction tissue, resulting in brittle stems that are prone to lodging [79,80,81,82]. In addition, varietal differences in lodging behavior are significant [9,83]. The planting of lodging-resistant varieties in production guarantees yield in stormy years. In maize, lodging-resistant cultivars (such as LI55, LI68, CX41) were found to withstand storms well without lodging, while the lodging rates of the sensitive cultivars (such as Chuan 273, Q1261, 14HF1994) were 20–42.9% [84]. Therefore, crop lodging resistance can be improved by appropriate land preparation, rational dense planting, adequate fertilization, the selection of lodging-resistant varieties, and the effective management of pests and diseases.

2.3. Genetic Factors Affecting Stem Lodging

Genotype is another important factor affecting stem lodging [37]. A number of studies have found that stem traits such as plant height, center of gravity, internode length at the base, stem thickness, stem cell wall thickness, stem stay-green degree, stem mechanical strength, stem bending stress, and stem components are affected by genetic factors, and are closely related to lodging resistance [85,86,87] (Figure 1). It is generally believed that increasing plant height increases the risk of crop lodging [2,7]. The first green revolution was advanced by the discovery of the semi-dwarf gene sd1, which was successfully introduced to reduce lodging and increase production indices in rice and barley [88,89,90,91]. Increase in plant height is generally considered to be the cause of lodging. However, this is not always applicable [1]. Tripathi et al. [9] reported some genotypes were lodging-resistant and some were susceptible despite being semi-dwarf spring wheat. Seri 82, UP 2338 and PBW 343 were assessed as tolerant while HD 2329 and Rayon 89 were susceptible to lodging. Gravity center height significantly affected the lodging resistance of maize. Li et al. [27] reported that compared to lodging-susceptible hybrid Xundan 20, lodging-resistant hybrid Denghai 605 showed a lower center of gravity that contributed to the higher lodging resistance of this hybrid. Regarding internode length, Sarker et al. [92] indicated a negative correlation between the length of the first internode and the lodging sensitivity, which further suggests that longer internodes at the base result in a higher lodging index. A quantitative trait locus was found to reduce culm internode length in barley, which further suggests that this QTL is also associated with reduced lodging [93]. There are significant differences in stem thickness and stem cell wall thickness among different lodging-resistant cultivars. The increase in stem thickness and cell wall thickness was found to be responsible for the enhancement of lodging resistance in SN9903 and YJ218 rice varieties [94]. Recently, a number of studies have shown that stay-green genotypes help to increase stalk lodging resistance under high planting density by reducing dry matter remobilization from the stalk [64,95]. The relationships between stem strength, stem rigidity and stem composition are complex and close [2,7,8]. It is generally believed that high stem or low lignin is detrimental to lodging resistance. An interesting report found that a long-culm variety, ‘Leaf Star’, with decreased lignin levels, has superior lodging resistance. Further research found that this variety has a thick layer of cortical fiber tissue with well-developed secondary cell walls [96]. In Arabidopsis thaliana, double-knockout mutants for NAC secondary wall thickening promoting factor 1 (NST1) and NST3 showed the loss of secondary walls in woody tissues, and nst1-1 nst3-1 plants were unable to stand upright [27,89,90,91]. To sum up, crop lodging is a complex agronomic trait, and resistance therefore needs to be addressed through enhancement at multiple levels.
Due to their mechanical characteristics, morphological characteristics and related genes of lodging-resistant stems have been introduced in previous reviews [1,2,7,37]. Therefore, in the following sections, we will focus on stem anatomy, stem composition, and the molecular regulatory networks of lignin, cellulose and hemicellulose in lodging-resistant crops.

2.4. Stem Anatomy and Lodging

Stem strength is one of the most important indicators used to evaluate lodging resistance. The anatomical characteristics of stem strength are closely related to the thickness of thick-walled tissues, the number of large vascular bundles, and sheath width [97,98]. Studies of the stem anatomy of rice, corn, and oats have found that the number and thickness of stem mechanical tissue layers, stem wall thickness, stem puncture strength, and the lignification of vascular bundles are significantly correlated with the ability to resist lodging. The number and area of small vascular bundles in the surrounding sclerenchyma of susceptible cultivars are lower than those of resistant cultivars [99,100,101]. Additionally, a smaller secondary xylem and phloem area is associated with a lower degree of cell wall lignification and thus with weaker lodging resistance [102]. The vascular bundle in the stem is a transport channel for water, minerals, and organic nutrients. Compared with susceptible varieties, lodging-resistant rice varieties have higher numbers of basal internode vascular bundles, thicker vascular bundle sheaths, an increased number of cell layers (which are more closely arranged), and higher levels of carbohydrate in the stem [103].
In summary, the intrinsic factors associated with lodging resistance are cell number, cell wall thickness, vascular bundle number, and the cell wall thickness of the stem mechanical tissues. To reduce lodging, these factors need to be further strengthened and the height and center of gravity of crop plants must be reduced.

2.5. Stem Components Affect Crop Lodging Resistance

The stem is a non-homogeneous structure consisting of the epidermis, mechanical tissue, thin-walled tissue, and vascular bundles; together, these comprise the main stress-bearing material of a plant. However, the vascular bundle of epidermal cells gradually loses protoplasm during its development, leaving only the cell wall; the physical construction of the stem tissue and the chemical composition of the cell wall are, therefore, the basis for resistance to bending [98,104,105]. Interestingly, carbon and nitrogen metabolism affect cell wall composition transition [106].
Lignin, cellulose, and hemicellulose are the main components of the stem stalk cell wall and secondary cell wall [25]. They play important roles in improving the mechanical strength of the stem and maintaining the stability of the cell wall [104,107]. In most cases, the three structural carbohydrates do not necessarily work together. It has been reported that lodging-resistant varieties contain a higher accumulation of lignin and cellulose in culms than those produced by lodging-susceptible varieties of soybeans. However, lodging-resistant varieties contain a lower accumulation of hemicellulose [108]. This may help to keep carbon sources stable. Interestingly, under the action of plant growth regulation, the lignin, cellulose and hemicellulose contents of maize stem could be significantly increased and significantly reduce the lodging percentage [109]. Some studies found that stem rigidity could increase anti-toppling load, but when the load exceeded the limit, breakage occurred easily. In contrast, soft, elastic stems were easily bent but not broken [110]. The modulus of elasticity of the homopolymer cellulose was found to be approximately 134 GPa in the axial direction under moist conditions. In contrast, matrix polymers, hemicellulose and lignin have a modulus of elasticity of 40 MPa and 2 GPa, respectively [111]. Therefore, cellulose and lignin play the main role in elasticity. The intrinsic relationship between stem tissue composition and lodging resistance is complex and requires further study.

2.5.1. Effects of Lignin on Lodging Resistance

The presence of lignin in the secondary cell wall can provide structural support to a plant. Lignin content is significantly correlated with the mechanical strength of the cell wall and the lodging resistance of the stem [112]. A report showed that the stem strength was mainly determined by lignin and cellulose contents. The lignin content in the stem had a greater effect on the stem strength compared to cellulose [23,108]. A large number of key enzymes for lignin synthesis have been discovered, among which, phenylalanine ammonia-lyase (PAL), caffeic acid O-methyltransferase (COMT), 4-coumarate coenzyme A ligase 3 (4CL3), cinnamyl alcohol dehydrogenase 2/7 (CAD2/7), cinnamoyl-CoA reductase 20 (CCR20), and cinnamate 4-hydroxylase (C4H) have been shown to increase lignin content and lodging resistance in plants [2,113]. Lignin-deficient mutants exhibit collapsed xylem and an inability to stand upright [114], and lignin content and associated enzyme activity are significantly correlated with the lodging resistance of barley stems [115]. The rapid expression of PAL, tyrosine ammonia-lyase (TAL), CAD, 4CL, and POD in the maize stem increases the induction of lignin synthesis and improves lodging resistance [116]. In addition, some studies have demonstrated that lignin content can be used as an indicator to evaluate the lodging resistance of crops [117,118]. These results suggest that lignin plays an important role in increasing the lodging resistance of crops.

2.5.2. Cellulose and Hemicellulose Influence Lodging Resistance

Stem development and lodging resistance mechanisms have previously been studied in crops such as rice [119], maize [120], wheat [19], brassica napus [121], and soybean [122]. It has been found that the cell wall and secondary cell wall components of the stem are important factors influencing the ability to resist lodging. Cellulose and hemicellulose influence the mechanical strength of crop stems. Cellulose, a glucose homopolymer composed of β-(1,4)-glucan chains, is the main component of the cell wall. Hemicellulose is a polysaccharide consisting mainly of xylose, glucose, or mannose [123]. Cellulose strengthens the stalk’s mechanical strength and reduces lodging. The increase in stem strength enhances the external force loaded by the stalk, so that the stalk is not easy to break (such as tearing, breaking and losing cohesion, etc.) [7]. As cellulose content decreases, soybean stems lose their mechanical strength and are more prone to lodging [124]. A previous study found that the cellulose content was higher in the stem of Jisu 19, a lodging-resistant foxtail millet cultivar, than in Xiaoxiangmi, a lodging-sensitive variety [121]. The cultivar Leaf Star with excellent lodging resistance was developed by increasing the content of cellulose and hemicellulose in rice. Leaf Star, developed from a cross between Koshihikari and Chugoku [116], has a high bending stress owing to its high densities of cellulose and hemicellulose in the culm compared to Koshihikari [125]. A comparable result was observed in hulless barley varieties. Zhao et al. [126] showed that the lodging-resistant variety Kunlun 14 had higher contents of cellulose and hemicellulose than the lodging-sensitive variety of Menyuanlianglan. Due to hemicellulose spatial organization and structural diversity, hemicellulose not only forms part of the matrix, but also acts as a coupling agent between the matrix and the hard cellulose fibrils [111]. A reduction in hemicellulose content was found to increase lodging resistance in soybean [108]. A given rice variety has high bending stress owing to high densities of hemicellulose and cellulose in the culm [125]. Therefore, we should focus on the important roles of cellulose and hemicellulose in crop lodging resistance.

2.5.3. Effects of Carbon and Nitrogen Metabolism on Lodging Resistance

Carbon and nitrogen metabolisms are significant intrinsic physiological factors that affect stem lodging [127]. Levels of lignin, cellulose, and hemicellulose gradually decrease with the increased application of nitrogen fertilizer, reducing the mechanical strength of the stem and increasing the lodging rate. Excess nitrogen significantly reduces the synthesis of H, G, and S lignin monomers and the total lignin content in maize; this demonstrates that the supply of nitrogen directly affects the composition and content of lignin in crops [107]. Levels of cellulose and lignin tend to be higher under low planting density and low nitrogen application conditions. Nitrogen fertilization and planting density above a specific threshold reduce stem bending strength [128]. Nitrogen fertilizer mainly affects the mechanical strength of the stem and increases the risk of lodging by reducing the degree of stem lignification, vascular bundle area, mechanical tissue thickness, and mechanical tissue cell wall thickness [66]. In addition, carbon and nitrogen metabolism, and especially the C/N ratio, play important roles in lodging resistance. High soluble sugar content improves the lodging resistance of crops, whereas a low C/N ratio leads to high nitrogen content and increased susceptibility to lodging [129]. Increasing stem lignification, vascular bundle area, and mechanical tissue thickness by regulating energy metabolism to enhance the hardness and toughness of stem materials is an effective way to improve stem strength and lodging resistance.
In summary, the proper regulation of lignin, cellulose, and hemicellulose synthesis can enhance plant resistance to lodging, as can the reasonable regulation of carbon and nitrogen sources.

3. Anti-Lodging Molecular Regulatory Network Controlling Lignin, Cellulose and Hemicellulose

3.1. Transcriptional Regulation of Lignin, Cellulose, and Hemicellulose

Genomic and molecular studies have identified a number of transcription factors involved in the synthesis of lignin, cellulose, and hemicellulose, and the synergistic transcriptional regulatory network is extremely complex [130,131,132,133,134]. NAC and MYB transcription factors are the master switches for secondary cell wall biosynthesis [25,135,136]. Previous studies have shown that the phosphorylation of an NAC transcription factor family member, the NAC secondary wall thickening promoting factor 1 (NST1), positively regulates secondary cell wall thickening in Arabidopsis fibroblasts. nst1 mutants also showed a drooping stem phenotype [137]. Xylem NAC domain 1 (XND 1) negatively regulates the deposition of secondary walls in xylem vessels by inhibiting vascular-related NAC domain (VND) proteins. In the VND knockout mutant lines, SND2, SND3, MYB46, MYB58, MYB63, MYB85, MYB103, and KNAT7 were all significantly down-regulated [138]. The expression of the secondary wall NAC domain (SWN) genes OsSWN and ZmSWN driven by the SND1 promoter in snd1 nst1 mutants effectively rescued the stem ptosis phenotype [139]. It has been reported that XND1 regulates xylem vessel secondary wall deposition by inhibiting VND function, and that transgenic SND1P::XND1 plants exhibit inflorescence stem lodging [138].
The NAC transcription factors SWN and MYB46 in rice and maize are target genes directly activated by the master transcriptional activators of the secondary wall biosynthesis program; this leads to the ectopic deposition of cellulose, xylan, and lignin, increasing stem mechanical strength [139,140]. The overexpression of MYB85 leads to the ectopic deposition of lignin in stem epidermal and cortical cells [141]. A transcription factor identified in Chinese white poplar (Populus tomentosa), PtoMYB170, can specifically activate the expression of genes related to lignin synthesis. Transgenic plants overexpressing PtoMYB170 have shown increased lignification and thickening of the xylem secondary cell wall, and plants bearing mutations in this gene are prone to lodging [142].
In summary, transcriptional regulation involves a complex network, with each level of regulation acting both independently and in cooperation with other levels. Only a small fraction of components related to secondary wall regulation have been shown to significantly affect lodging resistance. Therefore, the mining of key regulatory genes will be of great significance for the improvement of lodging resistance in crops.

3.2. Molecular Mechanisms of Lignin, Cellulose, and Hemicellulose Structural Genes in Resistance to Lodging

With the rapid development of molecular biological methods (such as genomics, metabolomics, proteomics, gene editing technology), several genes involved in the biosynthesis and assembly of lignin, cellulose, and hemicellulose have been identified through the study of mutants deficient in stem mechanical strength and cell wall structure. Lignin synthesis occurs mainly through three pathways: the phenylpyruvate metabolic pathway, the shikimic acid metabolic pathway, and the lignin synthesis-specific metabolic pathway; many genes that encode key enzymes from all three pathways have been identified [143,144,145]. PAL (encoding phenylalanine ammonia-lyase), COMT (encoding caffeic acid O-methyltransferase), 4CL3 (encoding 4-coumarate coenzyme A ligase 3), CAD2/7 (encoding cinnamyl alcohol dehydrogenase 2/7), CCR20 (encoding cinnamoyl-CoA reductase 20), and C4H (encoding cinnamate 4-hydroxylase) have all been shown to increase lignin content and lodging resistance in plants [106,112,146,147]. Lignin plays an important role in crop lodging resistance, especially by affecting the thickness of the cell wall and enhancing mechanical support in the stem. Many genes in the lignin synthesis pathway have been identified, but only some have been shown to play a role in crop lodging resistance. Wang et al. [148] have reported that the overexpression of TaCOMT-3D enhances stem mechanical strength and lignin (particularly syringyl monolignol) accumulation in the transgenic wheat lines. In wheat, Chen et al. [149] indicated the significant positive correlation between CAD gene expression and stem strength. Furthermore, Zhong et al. [138] found that NAC transcription factors regulate the expression of lignin synthesis genes. They employed the promoter of the fiber-specific secondary wall-associated NAC domain 1 (SND1) gene to ectopically express xylem NAC domain 1 (XND1) in Arabidopsis thaliana. The expression of XND1 under the SND1 promoter resulted in a pendent stem with the down-regulation of lignin-related genes (i.e., PAL1, HCT, CCoAOMT1). Therefore, further research into the roles and mechanisms of other lignin biosynthesis genes in lodging resistance should be conducted.
In recent years, rice brittle culm mutants (bc) have been found to be mainly characterized by atypical cellulose components; many related genes have been identified, such as bc1, bc3, bc6, bc10, and bc14 [20,150,151,152,153]. The bc1 gene belongs to the COBRA family, which functions in biological processes related to cell expansion and cell wall biosynthesis. In Arabidopsis, Zea mays, and Sorghum bicolor, COBRA-like 4 (AtCOBL4), brittle stem 2 (ZmBK2), and brittle culm1 (SbBC1), respectively, are involved in the biosynthesis of secondary cell wall cellulose and, therefore, greatly affect mechanical strength in the stem [154,155,156,157,158].
In higher plants, cellulose synthesis is usually catalyzed by the cellulose synthase (CESA) complex [159,160,161,162,163]. Cellulose crystallinity (CrI) is a key factor affecting the enzymatic saccharification of biomass and plant resistance to lodging. Mutations in cellulose synthase (CESA) 4, CESA8, and CESA9 reduce cellulose crystallinity in rice, remodeling the cell wall and improving lodging resistance [164,165]. The mutation of OsCESA4 increases lodging resistance by 17% [165]. In Arabidopsis, CesA8 drives the expression of sucrose synthase (SUS) 3, decreases cellulose crystallinity, and improves lodging resistance [165]. OsGH9B1, OsGH9B3, OsGH9B16, OsIRX9, and OsIRX14 negatively regulate cellulose crystallinity and positively regulate lodging resistance [164,166]. There are four main polymer forms of hemicellulose. Hemicellulose arabinose directly interacts with β-1, 4-glucan, which is the main factor affecting cellulose crystallinity. OSXAT2 and OSXAT3 promote the elongation of arabinose. The lignin G monomer can directly affect lodging resistance or indirectly interact with hemicellulose arabinose [166]. Further study of the cellulose and hemicellulose biosynthetic pathways will allow the identification of genes involved in the associated synthesis and regulatory pathways, providing valuable references for the study of crop lodging resistance.
In conclusion, many genes in the lignin, cellulose, and hemicellulose biosynthetic pathways have been identified, but only some genes have been proven to play a role in crop lodging resistance. We next describe recent advances in these three biosynthetic pathways to understand how they are regulated and how this knowledge can be used to improve cell wall properties, contributing to enhanced plant lodging resistance.

3.3. Agronomic Practices That Improve Levels of Lignin, Cellulose, and Hemicellulose

Agronomic management practices such as sowing depth [56,167], sowing density, fertilization and plant growth regulators (PGRs) [2,168,169,170] affect crop lodging. Some practices promote crop lodging resistance by enhancing levels of lignin, cellulose, and hemicellulose (Figure 2). One study indicated that deep sowing strengthened the anchorage of plants in the soil, thereby increasing lodging tolerance [171]. The first, second, and third basal internodes of rice planted by deep mechanical sowing substantially increased the breaking resistance of the stem bending moment of the rice panicle. A thicker culm wall, greater biomass accumulation, and greater lignin accumulation in the stem contributed to increased lodging resistance [167]. High planting density has been widely used to enhance grain production in crops, but supra-optimum planting density leads to an increase in lodging [62]. Li et al. [27] have reported that low planting densities contribute to stalk lignin accumulation, increase activities of lignin-associated enzymes, and increase mechanical strength, which ultimately reduces the lodging rate significantly.
In recent years, the effects of carbon and silicon fertilizers on crop lodging resistance have been studied [71,73,172,173,174,175]. Recent results have shown that both organic carbon and silicon fertilizers improve the activities of lignin biosynthesis enzymes (namely, PAL, 4CL, CAD, and peroxiredoxins) and the expression of related genes, increasing lignin accumulation in the culm and thus improving lodging resistance [72]. Silicon fertilizer treatment was found to improve single stem flexural strength and increase levels of silicon, lignin, and cellulose in rice stalks [176]. Levels of cellulose and acid detergent lignin were highest when silicon was applied at the reproductive and maturity stages [177]. This treatment affected the composition of plant cell wall components, mainly by altering linkages of non-cellulosic polymers and lignin [178]. K deficiency may be one of the contributing factors in lodging that leads to yield reduction [75,179]. K fertilization has been found to improve plant parameters such as basal internode space, cellulose content, and stem fiber content, which may also contribute to the ability of stems to withstand environmental stresses [76]. In contrast, the controlled release of nitrogen increases lignin and cellulose content, which improves lodging resistance [67,180,181]. However, in buckwheat, increased nitrogen fertilization significantly increased the risk of lodging by decreasing lignin content and related enzyme activities at the bottom of the second internode [182]. Optimized nitrogen fertilizer application rates significantly increased the activities of PAL, TAL, and POD in addition to lignin accumulation and culm lodging resistance [181].
The spraying of exogenous PGRs is an effective agronomic measure to combat lodging [183,184,185]. The magnitude and nature of lodging can be modified by applying growth regulators. Some regulators are employed to inhibit gibberellic acid biosynthesis pathways, while some are applied to produce more ethylene [1]. Asahina et al. [186] reported that uniconazole blocked gibberellin and brassinosteroid biosynthesis by attaching to cytochrome P450 monooxygenase. Uniconazole may facilitate the remodeling of stem components to improve stem strength. Fang et al. [72] found that the application of uniconazole significantly increased lignin content and the activities of PAL, 4CL, CAD, and POD in buckwheat. Paclobutrazol and chlormequat are important PGRs and antagonists of gibberellin. They function by inhibiting gibberellin biosynthesis, inhibiting cell elongation, and reducing lodging, which has been confirmed in barley, wheat, rice and oat [187,188,189]. Another important primary signal to regulate and to avoid lodging in plants is “ethylene”. Han et al. [190] indicated that ethylene had significant dwarfing effects on the stalk length and significantly reduced the lodging rate of sweet sorghum plants with a dose effect. Furthermore, N, N-Diethyl-2-hexanoyl oxygen radicals-ethyl amine (2-ethyl chloride) phosphonic acid salt (DHEAP, a single compound), a novel ethylene-like PGR, significantly reduced gibberellin contents in maize basal internodes and reduced maize lodging rates through reduced plant height and an improvement in cellulose content and lignin content [62]. In addition, a recent study has found that exogenous melatonin, as a new plant growth regulator, has a positive regulatory effect on stem strength [191]. Furthermore, Zhao et al. [191] found that supplementation with exogenous melatonin significantly enhanced stem strength by increasing lignin content and the S/G lignin compositional ratio. In contrast, the application of gibberellic acid had the opposite effects on stem characteristics. Exogenous GA3 reduced the accumulation of lignin and phenylalanine ammonia-lyase activity, which caused a significant lodging phenomenon in the lodging-resistant wheat variety [118].
The external environment changes the composition of lignin, cellulose, and hemicellulose largely by influencing the redistribution of carbon sources in the stem. A study found that the total concentration of cell wall components was negatively correlated with the non-structural carbohydrate concentration, indicating competition for carbon sources [192]. The application of the plant growth regulator simultaneously increases the contents of lignin, cellulose and hemicellulose, and reduced rice lodging. In contrast, shading increased non-structural carbohydrates (NSCs) and decreased structural carbohydrates (SCs), especially lignin, thus weakening stem stiffness. In summary, effective agronomic management practices can affect the carbon redistribution of stems, promote the synthesis of lignin, cellulose, and hemicellulose, and indirectly improve the lodging resistance of crops.

4. Future Prospects

Environmental factors affecting stem lodging; the anatomical features of culm lodging; lignin, cellulose and hemicellulose in relation to the lodging resistance of crops; and the genetic regulation of the mechanisms of lignin, cellulose and hemicellulose in relation to lodging resistance were reviewed. We found that environmental factors could affect the lodging capacity of crops by changing the composition of the stem by influencing carbon redistribution. Therefore, we propose that effective agronomic management practices can affect the carbon redistribution of stems, promote the synthesis of lignin, cellulose, and hemicellulose, and improve the lodging resistance of crops. However, how external environmental factors interact with internal genetic factors to influence crop lodging resistance remains to be further studied (Figure 3).
This study reveals the functions of key genes in the regulatory networks controlling the synthesis and metabolism of lignin, cellulose, and hemicellulose; the application of these genes in crop quality improvement has been discussed. These findings provide theoretical support for agricultural breeding. With improvements in molecular biological techniques and molecular markers, quantitative trait locus (QTL) mapping for the genetic foundations of crop lodging resistance can be conducted. An ethyl methanesulfonate (EMS) mutant library combined with efficient CRISPR/Cas9 technology would accelerate the identification of crop stem lodging resistance genes. Novel molecular breeding technologies and traditional gene cloning strategies can be combined to identify homologous genes in various species, allowing them to be broadly exploited in efforts to breed plants for lodging resistance.
Levels of lignin, cellulose, and hemicellulose in the stem play critical roles in improving the mechanical strength of the plant stem. Many studies have focused on the regulatory mechanisms of lodging beyond the purely physiological aspects. Plant lodging resistance is not regulated by a single signal transduction pathway, but rather by signals that interact with each other in a complex regulatory system. When plant lodging occurs, it affects the regulation of plant somatic cell formation, signal transduction, growth, development, and other physiological processes. However, the specific regulatory mechanisms remain unclear. This suggests that future studies related to crop lodging resistance should investigate stem development in more detail. With a great deal of research, the key metabolic steps of the lignin precursor biosynthesis pathway have gradually been discovered. However, the specific roles of lignin biosynthesis genes in lodging resistance require further research. At present, our understanding of the regulatory mechanisms affecting cellulose and hemicellulose is incomplete, meaning additional studies in this area are critical.
As more molecular markers related to stem strength are developed, crop stem strength can also be improved by aggregating multiple favorable alleles. Molecular polymerization breeding for stem strength can, therefore, be carried out by aggregating favorable alleles affecting either different traits related to stem strength or different loci for the same trait, thereby improving the efficiency of molecular breeding for crop lodging resistance.

Author Contributions

Conceptualization, Q.L. and L.O.; writing—original draft preparation, Q.L.; writing—review and editing, Q.L., C.F., C.L., X.N., X.Z., M.C. and L.O.; visualization, Q.L.; funding acquisition, L.O. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Natural Science Foundation of China, grant number 32172584 and Natural Science Foundation of Hunan, grant number 2021JJ30339.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Factors affecting stem lodging. The arrow means induction factors. The short line shows the lodging resistance factors.
Figure 1. Factors affecting stem lodging. The arrow means induction factors. The short line shows the lodging resistance factors.
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Figure 2. Agronomic practices affect stem components to resist lodging. All arrows indicate improvement. The red line represents suppression. PGRs—plant growth regulators. C, Si, K and N refer to carbon, silicon, potassium and nitrogen fertilizers, respectively.
Figure 2. Agronomic practices affect stem components to resist lodging. All arrows indicate improvement. The red line represents suppression. PGRs—plant growth regulators. C, Si, K and N refer to carbon, silicon, potassium and nitrogen fertilizers, respectively.
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Figure 3. Environmental and genetic factors influence stem cell wall components to improve crop lodging resistance. NACs—NAC family transcription factors; MYBs—MYB family transcription factors; NST—NAC secondary wall thickening promoting factor; SND—secondary wall-associated NAC domain protein; SWN—secondary wall NAC domain; XND—xylem NAC domain; VND—vascular-related NAC domain; KNAT—KNOTTED-like homeobox of Arabidopsis thaliana; SuSy—sucrose synthase; CesA—cellulose synthase; IRX—irregular xylem; XAT—xylan arabinosyltransferase; PAL—phenylalanine ammonia-lyase; 4CL—4-coumarate coenzyme A ligase; CAD—cinnamyl alcohol dehydrogenase; C4H—cinnamate 4-hydroxylase; CCR—cinnamoyl-CoA reductase; COMT—caffeic acid O-methyltransferase; CSE—caffeoyl shikimate esterase. The question mark indicates that the interaction between environmental factors and genetic factors in the study of lodging resistance mechanism needs to be further studied.
Figure 3. Environmental and genetic factors influence stem cell wall components to improve crop lodging resistance. NACs—NAC family transcription factors; MYBs—MYB family transcription factors; NST—NAC secondary wall thickening promoting factor; SND—secondary wall-associated NAC domain protein; SWN—secondary wall NAC domain; XND—xylem NAC domain; VND—vascular-related NAC domain; KNAT—KNOTTED-like homeobox of Arabidopsis thaliana; SuSy—sucrose synthase; CesA—cellulose synthase; IRX—irregular xylem; XAT—xylan arabinosyltransferase; PAL—phenylalanine ammonia-lyase; 4CL—4-coumarate coenzyme A ligase; CAD—cinnamyl alcohol dehydrogenase; C4H—cinnamate 4-hydroxylase; CCR—cinnamoyl-CoA reductase; COMT—caffeic acid O-methyltransferase; CSE—caffeoyl shikimate esterase. The question mark indicates that the interaction between environmental factors and genetic factors in the study of lodging resistance mechanism needs to be further studied.
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Li, Q.; Fu, C.; Liang, C.; Ni, X.; Zhao, X.; Chen, M.; Ou, L. Crop Lodging and The Roles of Lignin, Cellulose, and Hemicellulose in Lodging Resistance. Agronomy 2022, 12, 1795. https://doi.org/10.3390/agronomy12081795

AMA Style

Li Q, Fu C, Liang C, Ni X, Zhao X, Chen M, Ou L. Crop Lodging and The Roles of Lignin, Cellulose, and Hemicellulose in Lodging Resistance. Agronomy. 2022; 12(8):1795. https://doi.org/10.3390/agronomy12081795

Chicago/Turabian Style

Li, Qing, Canfang Fu, Chengliang Liang, Xiangjiang Ni, Xuanhua Zhao, Meng Chen, and Lijun Ou. 2022. "Crop Lodging and The Roles of Lignin, Cellulose, and Hemicellulose in Lodging Resistance" Agronomy 12, no. 8: 1795. https://doi.org/10.3390/agronomy12081795

APA Style

Li, Q., Fu, C., Liang, C., Ni, X., Zhao, X., Chen, M., & Ou, L. (2022). Crop Lodging and The Roles of Lignin, Cellulose, and Hemicellulose in Lodging Resistance. Agronomy, 12(8), 1795. https://doi.org/10.3390/agronomy12081795

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