Narrow-Leaf (dnl2) Mutant in Maize

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1		Xiaojiao Hu	+ 2036 word(s)	2036	2022-03-10 04:37:49	\|
2	format correct	Catherine Yang	Meta information modification	2036	2022-03-21 02:41:22	\|

This entry is adapted from the peer-reviewed paper 10.3390/ijms23020795

The dnl2 mutant is a recessive mutant caused by EMS mutagenesis that displays various developmental defects, with a short stature and narrowed leaves being the two most obvious features. Phenotypic and cytological observations revealed that narrow-leaf mutant, dnl2 showed inhibited cell growth, altered vascular bundle patterning, and disrupted secondary cell wall structure when compared with the wild-type, which could be the direct cause of the dwarf and narrow-leaf phenotype.

maize dnl2 mutant

1. Introduction

Maize (Zea mays L.) is one of the most important cereal crops in the world. Studies have demonstrated that increasing the planting density is an essential approach in order to increase per-hectare yield potential in maize ^[1]. However, a higher planting density can aggravate the lodging risk through increased plant height, leaf area, basal internode elongation, and center of gravity ^[2]^[3]. Plant height and leaf shape are important plant architecture traits that are closely associated with the lodging resistance, photosynthesis, and grain yield of maize ^[4]. The use of varieties with moderate plant height can enhance lodging resistance and improve the harvest index. With the popularization of short stature varieties during the green revolution, the yield of rice and wheat has increased sharply since the 1960s ^[5]. Leaf shape parameters, such as leaf length, leaf width, and leaf area, are important components of leaf morphology that affect canopy structure, photosynthetic efficiency, and wind circulation under high planting density ^[6]. Smaller and narrower leaves decrease shading effects on the lower leaves, enhance photosynthetically active radiation utilization, and increase maize yield potential ^[7]. Therefore, understanding the genetic mechanisms of maize plant height and leaf shape are important for the breeding of density-tolerant maize varieties with high grain yield.

Phytohormones, such as gibberellins (GAs), auxins (IAAs), ethylene (ETH), and brassinosteroids (BRs), play important roles in determining plant architecture traits, including plant height, leaf morphology, tiller number, and grain size ^[8]. For plant height, the previously characterized genes in maize are largely associated with the biosynthesis and the signal transduction of phytohormones. GAs represent a large group of cyclic diterpene compounds that are essential for stem elongation and plant height control ^[9]. GA synthesis, or signaling mutants, show dwarf phenotypes. The maize dwarf mutants, anther ear1 (an1), dwarf1 (d1), d3, and d5, have been shown to influence a different step in the biosynthesis of the GAs and are sensitive to exogenous GA application ^[10]^[11]^[12]^[13]. Two GA-insensitive dwarf mutants D8 and D9 were identified with altered DELLA domains, which are negative regulators of gibberellin signaling ^[14]^[15]. Auxin is an important signaling compound that is vital for plant development and growth ^[16]. VT2 encodes grass-specific tryptophan aminotransferase, the mutation of which affects IAA synthesis and causes dwarfing in maize ^[17]. Brachytic2 and ZmPIN1a regulate internode elongation by mediating the polar auxin transport in maize ^[18]^[19]. The overexpression of ZmPIN1a resulted in reduced plant height, ear height, and increased maize yield under high-density cultivation conditions ^[20]. In addition to the plant hormones GAs and IAAs, other phytohormones, such as BRs and ETH, also modulate plant height. Mutants that are deficient in BR biosynthesis or signal transduction, such as maize na1, na2, brd1, and the BRASSINOSTEROID INSENSITIVE1 knockdown line, exhibit the dwarfism phenotype ^[21]^[22]^[23]^[24]. The altered C-terminus of ZmACS7, encoding 1-aminocyclopropane-1-carboxylic acid (ACC) synthase in ETH biosynthesis, causes a shorter stature and larger leaf angle in maize ^[25].

Leaf width is an important index of leaf size and is a quantitative trait that is controlled by multiple genes, including miRNA, transcription factors, and hormones ^[26]. Genes that are related to response factors, polar transport, and the synthesis of phytohormones are believed to be particularly important in the regulation of leaf development in rice ^[27]. NAL7 (NARROW LEAF 7), TDD1 (TRYPTOPHAN DEFICIENT DWARF MUTANT 1), and FIB (FISH BONE) are involved in auxin biosynthesis, and the reduced expression of these genes results in a narrow-leaf phenotype ^[28]^[29]^[30]. The auxin-deficient mutants, defective in NAL1 (NARROW LEAF 1), NAL2/3, NAL21, OsARF11, and OsARF19, which participate in auxin polar transport, distribution, and signaling, also display narrow leaves ^[31]^[32]^[33]^[34]^[35]. Some genes that are involved in the regulation of the gibberellin pathway, such as PLA1, PLA2, SLR1, OsOFP2, D1, and GID2, have been shown to be important in the regulation of leaf width ^[11]^[36]^[37]^[38]^[39]. In addition to hormones, the cellulose synthase-like (CSL) genes, which participate in hemicellulose synthesis, are important in the regulation of leaf morphology ^[40]. DNL1, which encodes cellulose synthase-like D4, functions in the M-phase to regulate cell proliferation, and the dnl1 mutant showed a distinct narrow-leaf phenotype in rice ^[41]. ZmCSLD1 is essential for plant cell division, and the Zmcsld1 mutant exhibited narrow-organ and warty phenotypes with reduced cell sizes and cell numbers ^[42]. It is notable that narrow-leaf mutants commonly exhibit reduced plant height, such as nal1-2, nal1-3, nal21, dnl1, dnl2, and dnl3, implying the overlapping regulatory mechanisms of leaf size and plant height development.

2. Inhibited Cell Division and Expansion Result in the Dwarf and Narrow-Leaf Phenotypic of dnl2

Plant organ shape and size are precisely controlled by localized cell division and subsequent cell expansion during plant growth ^[43]. Extensive studies indicate that impaired mitosis, cell elongation, and expansion could result in a reduction in plant height, leaf area, and grain yield ^[44]^[45]^[46]. In rice, Dwarf1 (D1) encodes the α-subunit of the GTP-binding protein, which regulates cell division, promotes internode elongation, and influences plant height development ^[11]. The stemless dwarf 1 (STD1) encodes a phragmoplast-associated kinesin-related protein and has a fundamental role in cell division. The std1 mutant exhibited no differentiation of the node and internode organs, abnormal cell shapes, and a reduced cell division rate ^[47]. The Narrow leaf1 (NAL1) gene functions in cell division rather than cell elongation, and the nal1 mutant exhibited a dwarf and narrow-leaf phenotype with defective cell division ^[31]. In maize, Narrow Odd Dwarf (NOD) plays a cell-autonomous function. The nod mutants have smaller organs due to fewer and smaller cells ^[48]. In our study, the maize dnl2 mutant exhibited inhibited internode elongation and reduced leaf size. Internode elongation is driven by cell division in the intercalary meristem, followed by cell expansion in the elongation zone. A comparison of longitudinal sections taken from the dnl2 and wild-type internodes revealed that the parenchymal cells were irregularly shaped in dnl2, and both the cell length and width were significantly reduced compared to the wild-type, which suggested that cell elongation growth in the dnl2 internodes was suppressed. However, the cell number per unit was found to be significantly increased in dnl2, which could be an induced compensation phenomenon for the reduction in cell size. In the leaves, both the cell number and the cell width along the width direction of the leaf blade were decreased in dnl2 compared to the wild-type, while no significant change was observed in cell length. These results implied that the DNL2 gene has essential roles in cell proliferation and expansion. The reduced cell size and cell number are the major causes of the dwarf and narrow-leaf phenotype of dnl2.

Vascular bundle development is also an important determinant of plant height and leaf morphology. In rice, several mutants with reduced plant height and leaf width similar to that of dnl2 have been reported. Cross-section examination of the leaf blades of these mutants, such as nal1, nal7, nrl1, and tdd1, have demonstrated that narrow leaves mainly resulted from a defect in cell proliferation and a reduced number of vascular bundles ^[28]^[29]^[31]^[49]. In dnl2, altered vascular bundle patterning in the internodes and leaves was also observed. Compared with wild-type plants, the area of the vascular bundles was much smaller in the shortened internodes of dnl2, and the number of small veins was significantly reduced in the leaves of dnl2. The changed vascular bundle patterning in the internodes and leaves of dnl2 may be caused by either earlier defects in the recruitment of founder cells, or later defects in the differentiation of cells into vascular tissues, which suggested that the DNL2 gene was also crucial for determining vascular cell identity.

3. Altered Cell Wall Structure and Transcriptional Regulation Result in Defective Cell Growth in dnl2

Cell wall biosynthesis is important for regulating cell shape and size in the process of plant cell growth ^[50]. The change of vacuole turgor pressure is the main driving force in plant cell growth, and cell growth also depends on the synthesis and remodeling of cell wall polysaccharides ^[51]. In rice, the narrow leaf and dwarf1 (nd1) mutant exhibits significant growth inhibition due to suppressed cell division. Map-based cloning has revealed that the ND1 gene encodes OsCSLD4, which plays an important role in modifying the cell wall structure. The expression analysis revealed that OsCSLD4 is specifically expressed in M-phase cells in order to regulate cell proliferation ^[52]. ZmCSLD1 encodes an enzyme in cell wall biosynthesis and controls organ size by altering cell division. The inactivation of ZmCSLD1 also results in the narrow leaf and stunted phenotype mainly due to the decrease in cell number ^[42]. In our study, the thickness of the secondary cell wall of the vascular bundles in both the internodes and the leaves of dnl2 was significantly reduced compared to the wild-type. The histochemical staining results also indicated reduced lignin deposition in the secondary cell wall of dnl2. The altered cell wall structure may be related to the inhibited cell division and elongation.

During rapid cell growth, the development of new cell wall polymers relies on a large amount of cellulose and hemicellulose deposition, which is manipulated by the active expression of cell wall-related genes ^[53]^[54]. Transcriptome comparison between dnl2 and the wild-type showed that 66.7% of the 130 DEGs that are related to cell wall deposition and remodeling were down-regulated in dnl2 compared with the wild-type, especially the DEGs involved in secondary wall deposition. For example, CesA10, CesA11, CesA12, and Brittle stalk 2, which are abundant in the vascular bundles and are associated with secondary wall cellulose synthesis, were down-regulated by 2.2–7.2-fold. Twenty DEGs belong to GTs, GUXs, GXMs, and RWAS families, which participate in xylan synthesis and substitution, were also down-regulated. Additionally, 21 DEGs related to lignin synthesis were down-regulated, such as two PALs (Zm00001d003016, Zm00001d003015), which are the key enzymes of the phenylpropanoid pathway and exhibited 6.2–7.1-fold decreased expression levels. CCoAOMT (Zm00001d052841), which is involved in an alternative methylation pathway of lignin biosynthesis, was also decreased in expression by 4.8-fold. These expression changes explain the thinner secondary cell wall and decreased deposition of lignin around the vascular bundles and under the epidermis of dnl2 internodes and leaves.

4. Plant Hormones May Participate in the Regulation of Cell Growth and Vascular Patterning in dnl2

Plant growth and development are tightly regulated by phytohormones, such as auxin and gibberellin ^[55]. Auxin plays a pivotal role in regulating cell wall remodeling and overall cell growth ^[56]. Numerous mutants impaired in auxin synthesis or signaling exhibit overall dwarfism, defects in tropisms, and alterations in organ morphology ^[57]. In maize, loss-of-function of VANISHING TASSEL (VT2), which is a grass-specific IAA biosynthetic enzyme in the IPA pathway, shows shorter inflorescences and plant height due to defects in cell elongation ^[17]. The reduction in IAA levels gives rise to pleiotropic organ malformation together with a severe narrow-leaf phenotype in rice. The narrow leaf7 (nal7) mutant, which has a mutation in YUCCA8 (YUC8) that is involved in auxin synthesis, produces narrow and curly leaves throughout development ^[28]. NAL1 regulates the polar transport of auxin and modulates leaf size by affecting vein patterning and cell division ^[31]. Recent studies have shown that NAL2/3 not only regulates auxin distribution, but also has a negative feedback effect on gibberellin biosynthesis. It is suggested that NAL2/3 may regulate leaf size through the crosstalk between GA and auxin ^[32]. In both the nal1 and nal2/3 mutants, the number of small veins in the leaves is significantly reduced, whereas the number of large veins is only slightly reduced compared to the wild-type. In our study, dnl2 showed a significant decrease in the number of small veins compared with the wild-type plants. The GA and IAA contents were significantly decreased in both the internodes and the leaves of dnl2 relative to those of the wild-type. Therefore, we speculate that dnl2 has similar regulatory mechanisms as nal1 and nal2/3, caused by the crosstalk of IAA and GA. Our transcriptome results revealed that many genes involved in IAA and GA biosynthesis and signaling were differentially expressed between dnl2 and the wild-type plant. Flavin monooxygenase-like protein, which catalyzes the last step of conversion of IPyA to IAA, was down-regulated by 2.75-fold in dnl2. DWARF1, which encodes a gibberellin 3-oxidase that catalyzes the final step of bioactive GA synthesis, was also down-regulated by 6.43-fold in dnl2. Down-regulation of the expression of these genes could be the cause of the decreased IAA and GA contents in dnl2. Furthermore, auxin response gene families, such as Aux/IAA, GH3, SAUR, ARF, and PIN, and GA receptors exhibited altered expression in dnl2.

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