Abstract
Leaf morphology is critical for the survival of plant species. After a leaf primordium is initiated at the flank of shoot apical meristem (SAM), the development along the medial‐lateral direction enlarges the leaf‐blades, leading to the increase of photosynthetic activities. Thus, the revelation of mechanisms that control development across a leaf is quite important for plant breeding. A variety of narrow leaf mutants have been identified in the grass family, which includes particularly important crops in the world. Here, the molecular mechanisms underlying the leaf development in the medial‐lateral direction are discussed as we introduce the three major groups of narrow leaf mutants in the grass family: (1) auxin‐related mutants, (2) cellulose synthase‐like D (CSLD)‐related mutants, and (3) polarity‐related mutants. The results obtained from these analyses could be directly applied to the breeding of major cereal crops such as maize, rice, and barley; therefore, they could contribute to the increase of food production.
Keywords
- barley
- rice
- maize
- leaf morphogenesis
- mutant
- gene expression
1. Introduction
Leaves are the major photosynthetic organs in plants. The light‐capture efficiency significantly differs depending on the leaf shapes, angles, and arrangements in the canopy. Steeper leaf angle allows more light to penetrate to the lower leaves, leading to the increase of carbon gain through assimilation [1]. To avoid self‐shading, leaf arrangement (phyllotaxis) is highly regulated by the plant hormone auxin [2, 3]. Since carbohydrates used in living activities are largely derived from the photosynthesis in plants, leaf morphology is critical for the survival of plant species.
A leaf primordium is initiated at the flank of shoot apical meristem (SAM), in which cells are maintained an indeterminate state by
In SAMs, STM also downregulates the expression of the MYB transcription factor
The morphogenesis of sophisticated leaf organs with high reproducibility is achieved through the development in accordance with three axes; the proximal‐distal, adaxial‐abaxial, and medial‐lateral directions (Figure 1A–E) [8, 17]. The development along the medial‐lateral direction enlarges the leaf‐blades, leading to the increase of photosynthetic activities. Thus, the revelation of developmental mechanism along the medial‐lateral direction is quite important for plant breeding. So far, a variety of narrow leaf mutants have been identified in the grass family, which includes particularly important crops in the world. The results obtained from these analyses could be directly applied to the breeding of major crops such as maize, rice, and barley; therefore, they could contribute to the increase of food production. In fact, erect and narrow‐leafed rice mutants led to the higher photosynthetic CO2 uptake and improved yield in dense planting [18]. Recently, it was revealed that the Quantitative Trait Locus (QTL) controlling flag leaf morphology and photosynthetic activity were allelic to the causal gene for narrow leaf mutant in rice, suggesting the availability of narrow leaf genes for breeding high‐yield varieties [19–23].
Here, the molecular mechanisms underlying the leaf development in medial‐lateral direction are discussed as we introduce the three major groups of narrow leaf mutants in grass family: (1) auxin‐related mutants, (2) cellulose synthase‐like D (CSLD)‐related mutants, and (3) polarity‐related mutants.
2. Auxin‐related narrow leaf mutants
Auxin is a fundamental plant hormone and regulates a variety of plant growth and development. All parts of the young plant such as cotyledons, expanding leaves, and root tissues can potentially produce auxin although the youngest leaves exhibit the highest biosynthetic capacity [24–26]. Auxin is unique in its polar transportation (polar auxin transport (PAT)), as we mentioned above, mediated by influx carriers and efflux carriers [7]. The direction of auxin flow is the consequence of asymmetric localization of these carriers at plasma membrane [27, 28]. The resulting auxin localization within organs plays pivotal roles in phyllotactic patterning [29, 30], organogenesis [9, 31, 32], embryogenesis [33, 34], tropic response [35], and apical dominance [36]. At the cellular level, auxin regulates cell division, cell elongation, and cell differentiation [7, 37].
The predominant form of auxin is indole‐3‐acetic acid (IAA). Genetic and biochemical analyses indicated that tryptophan (Trp) is the main precursor of IAA in plants, and four biosynthetic pathways for IAA from Trp have been assumed [38–40]. Among IAA biosynthetic enzymes revealed so far, the most important biosynthetic enzymes are the tryptophan aminotransferase of arabidopsis (TAA) family of aminotransferases and the YUCCA (YUC) family of flavin‐containing monooxygenases [41, 42]. TAA1 catalyzes the conversion of Trp to indole‐3‐pyruvic acid (IPA) in the initial step of the IPA pathway, and YUC catalyzes the conversion of IPA to IAA, downstream of TAA, in
The importance of the IPA pathway in IAA biosynthesis is also demonstrated in grass family. In maize, loss‐of‐function of
The reduction in IAA levels gives rise to pleiotropic organ malformation together with severe narrow leaf phenotype in rice.
In contrast, rice
Overall, auxin‐related narrow leaf mutants exhibit pleiotropic abnormal phenotypes other than the reduction in leaf width. The representative phenotypes seem to be appeared in vascular patterning and root growth since auxin plays critical role in the development of these organs.
3. CSLD‐related narrow leaf mutants
Cell walls are essential structures surrounding plant cells. While cells are expanding, primary cell walls fulfill the support and barrier functions. After cell expansions are completed, secondary cell walls are formed between primary walls and plasma membranes, giving additional strength to cells. Cell wall is composed of polysaccharides, proteins, and phenolic compounds. Classically, polysaccharides are classified into cellulose, hemicelluloses, and pectins [56]. Cellulose synthase (CesA) protein contains a zinc finger domain at the
Based on the sequence similarity to
The uneven distribution of
In rice, inactivation of
The inactivation of
Overall,
4. Polarity‐related narrow leaf mutants
Most plant leaves are asymmetrical in all directions. Grass family leaves include leaf‐blade in the distal side, leaf‐sheath in the proximal side, and lamina‐joint between the leaf‐blade and leaf‐sheath. The bulliform cells, which curl leaf‐blades to prevent over transpiration, and xylems are formed only on the adaxial side, and the phloems on the abaxial side. The midrib, which functions as a physical support for the leaves, and ligule are formed in the medial side, and the sawtooth hairs and auricle in the lateral side (Figure 1A–E) [89]. For the construction of such a sophisticated organ, the proximal‐distal, adaxial‐abaxial, and medial‐lateral polarities must be constructed as soon as cells acquire leaf fate in SAM (Figures 1F and G).
Among the three polarities, the molecular mechanism of adaxial‐abaxial polarity is well studied using
While detail genetic regulators of proximal‐distal polarity remain unclear in
Compared with other polarities, the molecular mechanism of the medial‐lateral polarity is less understood. So far, it was revealed that
The nucleotide sequences of
The width of
While the medial‐lateral polarity is directly related to leaf width, mutation or over‐expression of the genes regulating the proximal‐distal or adaxial‐abaxial polarity can also result in the reduction in leaf width together with the alteration of organ polarities. Recessive mutant
On the other hand, Rice
Overall, polarity‐related narrow leaf mutants exhibit distinct reduction in leaf‐blade width together with the disruption of organ polarity. The loss‐of‐function of lateral identity is directly reflected in the reduction of leaf width, but the disruption of the proximal‐distal or adaxial‐abaxial polarities also affect the establishment or development along medial‐lateral axis, suggesting the interactive development between the three polarities.
5. Conclusion
The reduction in leaf width is a subtle morphological alteration, but the analyses of narrow leaf mutants have uncovered molecular functional diversity of the causal genes. Through a variety of genetic approaches, it has been demonstrated that
6. Materials and methods
6.1. Plant materials
For morphological observation of barley shoot, a wild type line Kanto Nijo 29 (KN29), which has two‐rowed spike and covered caryopsis, and its gamma‐ray induced
6.2. Paraffin sectioning and histological analysis
Plant samples were fixed with FAA (formaldehyde:glacial acetic acid:50% ethanol [2:1:17]) for 24 h at 4°C for histological analysis. They were then dehydrated in a graded ethanol series, substituted with 1‐butanol, and embedded in Paraplast® Plus (McCormick Scientific). The samples were sectioned at 8 μm thickness using a rotary microtome. For the histological analysis, sections were stained in hematoxylin or double‐stained in safranin and fast green. After staining, sections were mounted with Poly‐Mount® (Polysciences, Inc.) and observed with a light microscope.
6.3. Epidermal cell observation
The leaf‐blades were fixed with FAA (formaldehyde:glacial acetic acid:50% ethanol [2:1:17]) for 24h at 4°C. They were then dehydrated in a graded ethanol series. Dehydrated samples were incubated at 96°C in chloralhydrate dissolved in 100% ethanol until they were cleared, and observed with a light microscope.
6.4. Phylogenetic analysis
For the phylogenetic analysis of
References
- 1.
Falster DS, Westoby M. Leaf size and angle vary widely across species: What consequences for light interception?. New Phytologist. 2003; 158 :509‐525 - 2.
Hay A, Craft J, Tsiantis M. Plant hormones and homeoboxes: Bringing the gap?. BioEssays. 2004; 26 :395‐404 - 3.
Fleming AJ. Formation of primordia and phyllotaxy. Current opinion in Plant Biology. 2005; 8 :53‐58 - 4.
Hake S, Smith HMS, Holtan H, Magnani E, Mele G, Ramirez J. The role of KNOX genes in plant development. Annual Review of Cell and Developmental Biology. 2004; 20 :125‐151 - 5.
Hay A, Tsiantis M. KNOX genes: Versatile regulators of plant development and diversity. Development. 2010; 137 :3153‐3165 - 6.
Hepworth SR, Pautot VA. Beyond the divide: Boundaries for patterning and stem cell regulation in plants. Frontiers in Plant Science. 2015; 6 :1052 - 7.
Petrášek J, Friml J. Auxin transport routes in plant development. Development. 2009; 136 :2675‐2688 - 8.
Moon J, Hake S. How a leaf gets its shape. Current Opinion in Plant Biology. 2011; 14 :24‐30 - 9.
Křeček P, Skůpa P, Libus J, Naramoto S, Tejos R, Friml J, Zažímalová E. The PIN‐FORMED (PIN) protein family of auxin transporters. Genome Biology. 2009; 10 :249 - 10.
Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature. 2000; 408 :967‐971 - 11.
Guo M, Thomas J, Collins G, Timmermans MCP. Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. The Plant Cell. 2008; 20 :48‐58 - 12.
Li Z, Li B, Shen WH, Huang H, Dong A. TCP transcription factors interact with AS2 in the repression of class‐I KNOX genes in Arabidopsis thaliana. The Plant Journal. 2012; 71 :99‐107 - 13.
Hay A, Barkoulas M, Tsiantis M. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development. 2006; 133 :3955‐3961 - 14.
Tsiantis M, Hay A. Comparative plant development: the time of the leaf? Nature Reviews Genetics. 2003; 4 :169‐180 - 15.
Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E. The making of a compound leaf: Genetic manipulation of leaf architecture in tomato. Cell. 1996; 84 :735‐744 - 16.
Shani E, Burko Y, Ben‐Yaakov L, Berger Y, Amsellem Z, Goldshmidt A, Sharon E, Ori N. Stage‐specific regulation of Solanum lycopersicum leaf maturation by class 1 KNOTTED1‐LIKE HOMEOBOX proteins. The Plant Cell. 2009; 21 :3078‐3092 - 17.
Scarpella E, Barkoulas M, Tsiantis M. Control of leaf and vein development by auxin. Cold Spring Harbor Perspectives in Biology. 2010; 2 :a001511 - 18.
Yamaguchi H, Watanabe M, Sato S, Kanbayashi Y. Yielding ability of erect‐ and narrow‐leaved rice mutant in heavy manuring and dense planting culture. Radioisotopes. 1979; 28 :734‐738 - 19.
Chen M, Luo J, Shao G, Wei X, Tang S, Sheng Z, Song J, Hu P. Fine mapping of a major QTL for flag leaf width in rice, qFLW4, which might be caused by alternative splicing of NAL1. Plant Cell Reports. 2012; 31 :863‐872 - 20.
Fujita D, Trijatmiko KR, Tagle AG, Sapasap MV, Koide Y, Sasaki K, Tsakirpaloglou N, Gannaban RB, Nishimura T, Yanagihara S, Fukuta Y, Koshiba T, Slamet‐Loedin IH, Ishimaru T, Kobayashi N. NAL1 allele from a rice landrace greatly increases yield in modern indica cultivars. Proceedings of the National Academy of Sciences. 2013; 110 :20431‐20436 - 21.
Takai T, Adachi S, Taguchi‐Shiobara F, Sanoh‐Arai Y, Iwasawa N, Yoshinaga S, Hirose S, Taniguchi Y, Yamanouchi U, Wu J, Matsumoto T, Sugimoto K, Kondo K, Ikka T, Ando T, Kono I, Ito S, Shomura A, Ookawa T, Hirasawa T, Yano M, Kondo M, Yamamoto T. A natural variant of NAL1, selected in high‐yield rice breeding programs, pleiotropically increases photosynthesis rate. Scientific Reports. 2013; 3 :2149 - 22.
Zhang GH, Li SY, Wang L, Ye WJ, Zeng DL, Rao YC, Peng YL, Hu J, Yang YL, Xu, J, Ren DY, Gao ZY, Zhu L, Dong GJ, Hu XM, Yan MX, Guo LB, Li CY, Qian Q. LSCHL4 from Japonica Cultivar, which is allelic to NAL1, increases yield of indica super rice 93‐11. Molecular Plant. 2014; 7 :1350‐1364 - 23.
Taguchi‐Shiobara F, Ota T, Ebana K, Ookawa T, Yamasaki M, Tanabata T, Yamanouchi U, Wu J, Ono N, Nonoue Y, Nagata K, Fukuoka S, Hirabayashi H, Yamamoto T, Yano M. Natural variation in the flag leaf morphology of rice due to a mutation of the NARROW LEAF 1 gene in Oryza sativa L. genetics. 2015; 201 :795‐808 - 24.
Ljung K, Bhalerao RP, Sandberg G. Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. The Plant Journal. 2001; 28 :465‐474 - 25.
Benjamins R, Scheres B. Auxin: The looping star in plant development. Annu. Rev. Plant Biol. 2008; 59 :443‐465 - 26.
Finet C, Jaillais Y. AUXOLOGY: When auxin meets plant evo‐devo. Developmental Biology. 2012; 369 :19‐31 - 27.
Zažímalová E, Murphy A, Yang H, Hoyerová K, Hošek P. Auxin transporters: why so many?. Cold Spring Harbor Perspectives in Biology. 2010; 2 :a001552 - 28.
Leyser O. Auxin, self‐organisation, and the colonial nature of plants. Current Biology. 2011; 21 :331‐337 - 29.
Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J. PIN‐FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development. 2000; 127 :5157‐5165 - 30.
Bainbridge K, Guyomarc’h S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C. Auxin influx carriers stabilize phyllotactic patterning. Genes and Development. 2008; 22 :810‐823 - 31.
Scarpella E, Marcos D, Friml J, Berleth T. Control of leaf vascular patterning by polar auxin transport. Genes & Development. 2006; 20 :1015‐1027 - 32.
Kitomi Y, Ogawa A, Kitano H, Inukai Y. CRL4 regulates crown root formation through auxin transport in rice. Plant Root. 2008; 2 :19‐28 - 33.
Möller B, Weijers D. Auxin control of embryo patterning. Cold Spring Harbor Perspectives in Biology. 2009; 1 :a001545 - 34.
Forestan C, Meda S, Varotto S. ZmPIN1‐mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development. Plant Physiology. 2010; 152 :1373‐1390 - 35.
Mei Y, Jia WJ, Chu YJ, Xue HW. Arabidopsis phosphatidylinositol monophosphate 5‐kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins. Cell Research. 2012; 22 :581‐597 - 36.
Prusinkiewicz P, Crawford S, Smith RS, Ljung K, Bennett T, Ongaro V, Leyser O. Control of bud activation by an auxin transport switch. Proceedings of the National Academy of Sciences. 2009; 106 :17431‐17436 - 37.
Vanneste S, Friml J. Auxin: A trigger for change in plant development. Cell. 2009; 136 :1005‐1016 - 38.
Sugawara S, Hishiyama S, Jikumaru Y, Hanada A, Nishimura T, Koshiba T, Zhao Y, Kamiya Y, Kasahara H. Biochemical analyses of indole‐3‐acetaldoxime‐dependent auxin biosynthesis in Arabidopsis. Proceedings of the National Academy of Sciences. 2009; 106 :5430‐5435 - 39.
Zhao Y. Auxin biosynthesis and its role in plant development. Annual Review of Plant Biology. 2010; 61 :49‐64 - 40.
Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, McSteen P, Zhao Y, Hayashi K, Kamiya Y, Kasahara H. The main auxin biosynthesis pathway in Arabidopsis. Proceedings of the National Academy of Sciences. 2011; 108 :18512‐18517 - 41.
Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J. A role for flavin monooxygenase‐like enzymes in auxin biosynthesis. Science. 2001; 291 :306‐309 - 42.
Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y. Conversion of tryptophan to indole‐3‐acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proceedings of the National Academy of Sciences. 2011; 108 :18518‐18523 - 43.
Stepanova AN, Robertson‐Hoyt J, Yun J, Benavente LM, Xie DY, Doležal K, Schlereth A, Jürgens G, Alonso JM. TAA1‐mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 2008; 133 :177‐191 - 44.
Stepanova AN, Yun J, Robles LM, Novak O, He W, Guo H, Ljung K, Alonso JM. The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole‐3‐pyruvic acid branch of auxin biosynthesis. The Plant Cell. 2011; 23 :3961‐3973 - 45.
Dai X, Mashiguchi K, Chen Q, Kasahara H, Kamiya Y, Ojha S, DuBois J, Ballou D, Zhao Y. The biochemical mechanism of auxin biosynthesis by an Arabidopsis YUCCA flavin‐containing monooxygenase. Journal of Biological Chemistry. 2013; 288 :1448‐1457 - 46.
Cheng Y, Dai X, Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes and Development. 2006; 20 :1790‐1799 - 47.
Gallavotti A, Barazesh S, Malcomber S, Hall D, Jackson D, Schmidt RJ, McSteen P. sparse inflorescence 1 encodes a monocot‐specific YUCCA‐like gene required for vegetative and reproductive development in maize. Proceedings of the National Academy of Sciences. 2008; 105 :15196‐15201 - 48.
Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL, Hudson C, Barazesh S, Cohen JD, Malcomber S, McSteen P. vanishing tassel 2 encodes a grass‐specific Tryptophan Aminotransferase required for vegetative and reproductive development in maize. The Plant Cell. 2011; 23 :550‐566 - 49.
Fujino K, Matsuda Y, Ozawa K, Takeshi N, Koshiba T, Fraaije MW, Sekiguchi H. NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Molecular Genetics and Genomics. 2008; 279 :499‐507 - 50.
Yoshikawa T, Ito M, Sumikura T, Nakayama A, Nishimura T, Kitano H, Yamaguchi I, Koshiba T, Hibara K, Nagato Y, Itoh J. The rice FISH BONE gene encodes a tryptophan aminotransferase, which affects pleiotropic auxin‐related processes. The Plant Journal. 2014; 78 :927‐936 - 51.
Sazuka T, Kamiya N, Nishimura T, Ohmae K, Sato Y, Imamura K, Nagato Y, KoshibaT, Nagamura Y, Ashikari M, Kitano H, Matsuoka M. A rice tryptophan deficient dwarf mutant, tdd1, contains a reduced level of indole acetic acid and develops abnormal flowers and organless embryos. The Plant Journal. 2009; 60 :227‐241 - 52.
Woo YM, Park HJ, Su’udi M, Yang JI, Park JJ, Back K, Park YM, An G. Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio. Plant Molecular Biology. 2007; 65 :125‐136 - 53.
Abu‐Zaitoon YM, Bennett K, Normanly J, Nonhebel HM. A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain‐specific YUCCA. Physiologia Plantarum. 2012; 146 :487‐499 - 54.
Qi J, Qian Q, Bu Q, Li S, Chen Q, Sun J, Liang W, Zhou Y, Chu C, Li X, Ren F, Palme K, Zhao B, Chen J, Chen M, Li C. Mutation of the rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiology. 2008; 147 :1947‐1959 - 55.
Jiang D, Fang J, Lou L, Zhao J, Yuan S, Yin L, Sun W, Peng L, Guo B, Li X. Characterization of a null allelic mutant of the rice NAL1 gene reveals its role in regulating cell division. PLoS ONE. 2015; 10 . DOI: 10.1371/journal.pone.0118169 - 56.
Scheller HV, Ulvskov P. Hemicelluloses. Annual Review of Plant Biology. 2010; 61 :263‐289 - 57.
Richmond T. Higher plant cellulose synthases. Genome Biology. 2000; 1 :reviews3001.1‐1.6. - 58.
Kurek I, Kawagoe Y, Jacob‐Wilk D, Doblin M, Delmer D. Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc‐binding domains. Proceedings of the National Academy of Sciences. 2002; 99 :11109‐11114 - 59.
Taylor NG. Cellulose biosynthesis and deposition in higher plants. New Phytologist. 2008; 178: 239‐252 - 60.
Richmond TA, Somerville CR. The cellulose synthase superfamily. Plant Physiology. 2000; 124 :495‐498 - 61.
Hazen SP, Scott‐Craig JS, Walton JD. Cellulose synthase‐like genes of rice. Plant Physiology. 2002; 128 :336‐340 - 62.
Fincher GB. Revolutionary times in our understanding of cell wall biosynthesis and remodeling in the grasses. Plant Physiology. 2009; 149 :27‐37 - 63.
Dhugga KS, Barreiro R, Whitten B, Stecca K, Hazebroek J, Randhawa GS, Dolan M, Kinney AJ, Tomes D, Nichols S, Anderson P. Guar seed beta‐mannan synthase is a member of the cellulose synthase super gene family. Science. 2004; 303 :363‐366 - 64.
Liepman AH, Wilkerson CG, Keegstra K. Expression of cellulose synthase‐like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. Proceedings of the National Academy of Sciences. 2005; 102 :2221‐2226 - 65.
Suzuki S, Li L, Sun YH, Chiang VL. The cellulose synthase gene superfamily and biochemical functions of xylem‐specific cellulose synthase‐like genes in Populus trichocarpa. Plant Physiology. 2006; 142 :1233‐1245 - 66.
Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB. Cellulose synthase‐like CslF genes mediate the synthesis of cell wall (1,3;1,4)‐beta‐D‐glucans. Science. 2006; 311 :1940‐1942 - 67.
Doblin MS, Pettolino FA, Wilson SM, Campbell R, Burton RA, Fincher GB, Newbigin E, Bacic A. A barley cellulose synthase‐like CSLH gene mediates (1,3;1,4)‐beta‐D‐glucan synthesis in transgenic Arabidopsis. Proceedings of the National Academy of Sciences. 2009; 106 :5996‐6001 - 68.
Cocuron JC, Lerouxel O, Drakakaki G, Alonso AP, Liepman AH, Keegstra K, Raikhel N, Wilkerson CG. A gene from the cellulose synthase‐like C family encodes a β‐1,4‐glucan synthase. Proceedings of the National Academy of Sciences. 2007; 104 :8550‐8555 - 69.
Dwivany FM, Yulia D, Burton RA, Shirley NJ, Wilson SM, Fincher GB, Bacic A, Newbigin E, Doblin MS. The Cellulose‐synthase like C (CslC) family of barley includes members that are integral membrane proteins targeted to the plasma membrane. Molecular Plant. 2009; 2 :1025‐1039 - 70.
Roberts AW, Bushoven JT. The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens. Plant Molecular Biology. 2007; 63 :207‐219 - 71.
Hunter CT, Kirienko DH, Sylvester AW, Peter GF, McCarty DR, Koch KE. Cellulose synthase‐like D1 is integral to normal cell division, expansion, and leaf development in maize. Plant Physiology. 2012; 158 :708‐724 - 72.
Yoshikawa T, Eiguchi M, Hibara K, Ito J, Nagato Y. Rice SLENDER LEAF1 gene encodes cellulose synthase‐like D4 and is specifically expressed in M‐phase cells to regulate cell proliferation. Journal of Experimental Botany. 2013; 64 :2049‐2061 - 73.
Bernal AJ, Yoo CM, Mutwil M, Jensen JK, Hou G, Blaukopf C, Sørensen I, Blancaflor EB, Scheller HV, Willats WGT. Functional analysis of the cellulose synthase‐like genes Csld1, Csld2, and Csld4 in tip‐growing Arabidopsis cells. Plant Physiology. 2008; 148 :1238‐1253 - 74.
Favery B, Ryan E, Foreman J, Linstead P, Boundonck K, Steer M, Shaw P, Dolan L. KOJAK encodes a cellulose synthase‐like protein required for root hair cell morphogenesis in Arabidopsis. Genes and Development. 2001; 15 :79‐89 - 75.
Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M, Van Lijsebettens M. AtCSLD3, a cellulose synthase‐like gene important for root hair growth in Arabidopsis. Plant Physiology. 2001; 126 :575‐586 - 76.
Kim CM, Park SH, Je BI, Park SH, Park SJ, Piao HL, Eun MY, Dolan L, Han C. OsCsld1, a cellulose synthase‐like D1 gene, is required for root hair morphogenesis in rice. Plant Physiology. 2007; 143 :1220‐1230 - 77.
Penning BW, Hunter CTIII, Tyengwa R, Eveland AL, Dugard CK, Olek AT, Vermerris W, Koch KE, McCarty DR, Davis MF, Thomas SR, McCann MC, Carpita NC. Genetic resources for maize cell wall biology. Plant Physiology. 2009; 151 :1703‐1728 - 78.
Li M, Xiong G, Li R, Cui J, Tang D, Zhang B, Pauly M, Cheng Z, Zhou Y. Rice cellulose synthase‐like D4 is essential for normal cell‐wall biosynthesis and plant growth. The Plant Journal. 2009; 60 :1055‐1069 - 79.
Hu J, Zhu L, Zeng D, Gao Z, Guo L, Fang Y, Zhang G, Dong G, Yan M, Liu J, Qian Q. Identification and characterization of NARROW AND ROLLED LEAF 1, a novel gene regulating leaf morphology and plant architecture in rice. Plant Molecular Biology. 2010; 73 :283‐292 - 80.
Luan W, Liu Y, Zhang F, Song Y, Wang Z, Peng Y, Sun Z. OsCD1 encodes a putative member of the cellulose synthase‐like D sub‐family and is essential for rice plant architecture and growth. Plant Biotechnology Journal. 2010; 9 :513‐524 - 81.
Ding Z, Lin Z, Li Q, Wu H, Xiang C, Wang J. DNL1, encodes cellulose synthase‐like D4, is a major QTL for plant height and leaf width in rice (Oryza sativa L.). Biochemical and Biophysical Research Communications. 2015; 457 :133‐140 - 82.
Shi L, Wei XJ, Adedze YM, Sheng ZH, Tang SQ, Hu PS, Wang JL. Characterization and gene cloning of the rice (Oryza sativa L.) dwarf and narrow‐leaf mutant dnl3. Genetics and Molecular Research. 2016; 15 . DOI: 10.4238/gmr.15038731 - 83.
Horiguchi G, Tsukaya H. Organ size regulation in plants: insights from compensation. Frontiers in Plant Science. 2011; 2 :1‐6 - 84.
Lukowitz W, Mayer U, Jügens G. Cytokinesis in the Arabidopsis embryo involves the synthaxin‐related KNOLLE gene proruct. Cell. 1996; 84 :61‐71 - 85.
Zuo J, Niu QW, Nishizawa N, Wu Y, Kost B, Chua NH. KORRIGAN, an Arabidopsis endo‐1,4‐β‐glucanase, localizes to the cell plate by polarized ta‐getting and is essential for cytokinesis. The Plant Cell. 2000; 12 :1137‐1152 - 86.
Strompen G, Kasmi FE, Richter S, Lukowitz W, Assaad FF, Jügens G, Mayer U. The Arabidopsis HINKEL gene encodes a kinesin‐related protein involved in cytokinesis and is expressed in a cell cycle‐dependent manner. Current Biology. 2002; 12 :153‐158 - 87.
Yin L, Verhertbruggen Y, Oikawa A, Manisseri C, Knierim B, Prak L, Jensen JK, Knox JP, Auer M, Willats WGT, Scheller HV. The cooporative activities of CSLD2, CSLD3, and CSLD5 are required for normal Arabidopsis development. Molecular Plant. 2011; 4 :1024‐1037 - 88.
Goubet F, Barton CJ, Mortimer JC, Yu X, Zhang Z, Miles GP, Richens J, Liepman AH, Seffen K, Dupree P. Cell wall glucomannan in Arabidopsis is synthesised by CSLA glycosyltransferases, and influences the progression of embryogenesis. Plant J. 2009; 60 :527‐538 - 89.
Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y. Rice plant development: from zygote to spikelet. Plant Cell Physiol. 2005; 46 :23‐47 - 90.
Nakata M, Okada K. The leaf adaxial‐abaxial boundary and lamina growth. Plants. 2013; 2 :174‐202 - 91.
Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 2005; 15 :1899‐1911 - 92.
Vernoux T, Besnard F, Traas J. Auxin at the shoot apical meristem. Cold Spring Harbor Perspectives in Biology. 2010; 2 :a001487 - 93.
Yan S, Yan CJ, Zeng XH, Yang YC, Fang YW, Tian CY, Sun YW, Cheng ZK, Gu MH. ROLLED LEAF 9, encoding a GARP protein, regulates the leaf abaxial cell fate in rice. Plant Molecular Biology. 2008; 68 :239‐250 - 94.
Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW. SHALLOT‐LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell. 2009; 21 :719‐735 - 95.
Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC. microRNA‐mediated repression of rolled leaf1 specifies maize leaf polarity. Nature. 2004; 428 :84‐88 - 96.
Freeling M. A conceptual framework for maize leaf development. Journal of Developmental Biology. 1992; 153 :44‐58 - 97.
Sinha N, Hake S. The Knotted leaf blade is a mosaic of blade, sheath, and auricle identities. Developmental Genetics Journal. 1994; 15 :401‐414 - 98.
Vollbrecht E, Veit B, Sinha N, Hake S. The developmental gene Knotted‐1 is a member of a maize homeobox gene family. Nature. 1991; 350 :241‐243 - 99.
Smith L, Greene B, Veit B, Hake S. A dominant mutation in the maize homeobox gene, knotted‐1, causes its ectopic expression in leaf cells with altered fates. Development. 1992; 116 :21‐30 - 100.
Jackson D, Veit B, Hake S. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development. 1994; 120 :405‐413 - 101.
Foster T, Veit B, Hake S. Mosaic analysis of the dominant mutant, Gnarley1‐R, reveals distinct lateral and transverse signaling pathways during maize leaf development. Development. 1999; 126 :305‐313 - 102.
Ramirez J, Bolduc N, Lisch D, Hake S. Distal expression of knotted1 in maize leaves leads to reestablishment of proximal/distal patterning and leaf dissection. Plant Physiology. 2009; 151 :1878‐1888 - 103.
Müller KJ, Romano N, Gerstner O, Garcia‐Maroto F, Pozzi C, Salamini F, Rohde W. The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature. 1995; 374 :727‐730 - 104.
Schneeberger RG, Becraft PW, Hake S, Freeling M. Ectopic expression of the knox homeo box gene rough sheath1 alters cell fate in the maize leaf. Genes & Development. 1995; 9 :2292‐2304 - 105.
Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG. The BLADE‐ON‐PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development. 2003; 130 :161‐172 - 106.
Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C. Integration of transportbased models for phyllotaxis and midvein formation. Genes & Development. 2009; 23 :373-384 - 107.
Becraft PW, Bongard‐Pierce DK, Sylvester AW, Poethig RS, Freeling M. The liguleless‐1 gene acts tissue specifically in maize leaf development. Developmental Biology. 1990; 141 :220‐232 - 108.
Becraft PW, Freeling M. Sectors of liguleless‐1 tissue interrupt an inductive signal during maize leaf development. Plant Cell. 1991; 3 :801‐807 - 109.
Harper L, Freeling M. Interactions of liguleless1 and liguleless2 function during ligule induction in maize. Genetics. 1996; 144 :1871‐1882 - 110.
Moreno MA, Harper LC, Krueger RW, Dellaporta SL, Freeling M. liguleless1 encodes a nuclear‐localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes & Development. 1997; 11 :616‐628 - 111.
Walsh J, Water CA, Freeling M. The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade‐sheath boundary. Genes & Development. 1998; 12 :208‐218 - 112.
Foster T, Hay A, Johnston R, Hake S. The establishment of axial patterning in the maize leaf. Development. 2004; 131 :3921‐3929 - 113.
Johnston R, Wang M, Sun Q, Sylvester AW, Hake S, Scanlon MJ. Transcriptomic analyses indicate that maize ligule development recapitulates gene expression patterns that occur during lateral organ initiation. Plant Cell. 2014; 26 :4718‐4732 - 114.
Muehlbauer GJ, Fowler JE, Girard L, Tyers R, Harper L, Freeling M. Ectopic expression of the maize homeobox gene liguleless3 alters cell fates in the leaf. Plant Physiol. 1999; 119 :651‐662 - 115.
Bauer P, Lubkowitz M, Tyers R, Nemoto K, Meeley RB, Goff SA, Freeling M. Regulation and a conserved intron sequence of liguleless3/4 knox class‐I homeobox genes in grasses. Planta. 2004; 219 :359‐368 - 116.
Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY. The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell. 2004; 16 :500‐509 - 117.
Nardmann J, Ji J, Werr W, Scanlon MJ. The maize duplicated genes narrow sheath1 and narrow sheath2 encodes a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development. 2004; 131 :2827‐2839 - 118.
Scanlon MJ, Freeling M. The narrow sheath leaf domain: a genetic tool used to reveal developmental homologies among modified maize organs. The Plant Journal. 1998; 13 :547‐561 - 119.
Scanlon MJ, Schneeberger RG, Freeling M. The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development. 1996; 122 :1683‐1691 - 120.
Scanlon MJ. NARROW SHEATH1 functions from two meristematic foci during founder‐cell recruitment in maize leaf development. Development. 2000; 127 :4573‐4585 - 121.
Scanlon MJ, Freeling M. Clonal sectors reveal that a specific meristematic domain is not utilized in the maize mutant narrow sheath. Developmental Biology. 1997; 182 :52‐66 - 122.
Scanlon MJ, Chen KD, McKnight IV CC. The narrow sheath duplicate gene: sectors of dual aneuploidy reveal ancestrally conserved gene functions during maize leaf development. Genetics. 2000; 155 :1379‐1389 - 123.
Yoshikawa T, Tanaka SY, Masumoto Y, Nobori N, Ishii H, Hibara K, Itoh J, Tanisaka T, Taketa S. Barley NARROW LEAFED DWARF1 encoding a WUSCHEL‐RELATED HOMEOBOX 3 (WOX3) regulates the marginal development of lateral organs. Breeding Science. 2016; 66 :416‐424 - 124.
The Rice Chromosomes 11 and 12 Sequencing Consortia. The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biology. 2005; 3 :20 - 125.
Cho SH, Yoo SC, Zhang H, Pandeya D, Koh HJ, Hwang JY, Kim GT, Paek NC. The rice narrow leaf2 and narrow leaf3 loci encode WUSCHEL‐related homeobox 3A (OsWOX3A) and function in leaf, spikelet, tiller and lateral root development. New Phytologist. 2013; 198 :1071‐1084 - 126.
Ishiwata A, Ozawa M, Nagasaki H, Kato M, Noda Y, Yamaguchi T, Nosaka M, Shimizu‐Sato S, Nagasaki A, Maekawa M, Hirano HY, Sato Y. Two WUSCHEL‐related homeobox genes, narrow leaf2 and narrow leaf3, control leaf width in rice. Plant Cell Physiol. 2013; 54 :779‐792 - 127.
Troll W. Concerning the morphological significance of the so‐called vorlaeuferspitze of monocot leaves. A contribution to the typology of monocot leaves. Beitr. Biol. Pflanz. 1955; 31 :525‐558 - 128.
Haecker A, Gross‐Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development. 2004; 131 :657‐668 - 129.
Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema AS, Gerats T. Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell. 2009; 21 :2269‐2283 - 130.
Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K. Roles of the middle domain‐specific WUSCHEL‐RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell. 2012; 24 :519‐535 - 131.
Schneeberger R, Tsiantis M, Freeling M, Langdale JA. The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development. 1998; 125 :2857‐2865 - 132.
Moon J, Candela H, Hake S. The Liguleless narrow mutation affects proximal‐distal signaling and leaf growth. Development. 2013; 140 :405‐412 - 133.
Hay A, Hake S. The dominant mutant Wavy auricle in blade1 disrupts patterning in a lateral domain of the maize leaf. Plant Physiol. 2004; 135 :300‐308 - 134.
Lewis MW, Bolduc N, Hake K, Htike Y, Hay A, Candela H, Hake S. Gene regulatory interactions at lateral organ boundaries in maize. Development. 2014; 141 :4590‐4597 - 135.
Liu X, Li M, Liu K, Tang D, Sun M, Li Y, Shen Y, Du G, Cheng Z. Semi‐Rolled Leaf 2 modulates rice leaf rolling by regulating abaxial side cell differentiation. Journal of Experimental Botany. 2016; 67 :2139‐2150 - 136.
Li YY, Shen A, Xiong W, Sun QL, Luo Q, Song T, Li ZL, Luan WJ. Overexpression of OsHox32 results in pleiotropic effects on plant type architecture and leaf development in rice. Rice. 2016; 9 :46. DOI: 10.1186/s12284‐016‐0118‐1 - 137.
Li C, Zou X, Zhang C, Shao Q, Liu J, Liu B, Li H, Zhao T. OsLBD3‐7 Overexpression induced adaxially rolled leaves in rice. PLoS One. 2016; 11 :e0156413. DOI: 10.1371/journal.pone.0156413 - 138.
Henderson DC, Muehlbauer GJ, Scanlon MJ. Radial leaves of the maize mutant ragged seedling2 retain dorsiventral anatomy. Developmental Biology. 2005; 282 :455‐466 - 139.
Itoh J, Sato Y, Nagato Y. The SHOOT ORGANIZATION2 gene coordinates leaf domain development along the central‐marginal axis in rice. Plant Cell Physiol. 2008; 49 :1226‐1236 - 140.
Timmermans MC, Schultes NP, Jankovsky JP, Nelson T. Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development. 1998; 125 :2813‐2823 - 141.
Nogueira FT, Madi S, Chitwood DH, Juarez MT, Timmermans MC. Two small regulatory RNAs establish opposing fates of a developmental axis. Genes & Development. 2007; 21 :750‐755 - 142.
Satoh N, Itoh J, Nagato Y. The SHOOTLESS2 and SHOOTLESS1 genes are involved in both initiation and maintenance of the shoot apical meristem through regulating the number of indeterminate cells. Genetics. 2003; 164 :335‐346 - 143.
Nagasaki H, Itoh J, Hayashi K, Hibara K, Satoh‐Nagasawa N, Nosaka M, MukouhataM, Ashikari M, Kitano H, Matsuoka M, Nagato Y, Sato Y. The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proceedings of the National Academy of Sciences. 2007; 104 :14867‐14871 - 144.
Itoh JI, Kitano H, Matsuoka M, Nagato Y. Shoot organization genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell. 2000; 12 :2161‐2174 - 145.
Sarojam R, Sappl PG, Goldshmidt A, Efroni I, Floyd SK, Eshed Y, Bowman JK. Differentiating Arabidopsis shoots from leaves by combined YABBY activities. Plant Cell. 2010; 22 :2113‐2130 - 146.
Stahle MI, Kuehlich J, Staron L, von Arnim AG, Golz JF. YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell. 2009; 21 :3105‐3118 - 147.
Wang W, Xu B, Wang H, Li J, Huang H, Xu L. YUCCA genes are expressed in response to leaf adaxial‐abaxial juxtaposition and are required for leaf margin development. Plant Physiol. 2011; 157 :1805-1819 - 148.
Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution. 2016; 33 :1870‐1874