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How Histocytes Modulate Leaf Polarity Establishment

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How Histocytes Modulate Leaf Polarity Establishment Available online at www.sciencedirect.com ScienceDirect Rice Science, 2020, 27(6): 468−479 Review Development of Rice Leaves: How Histocytes Modulate Leaf Polarity Establishment # # WANG Jiajia , XU Jing , QIAN Qian, ZHANG Guangheng (State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou 310006, China; #These authors contributed equally to this work) Abstract: An ideal leaf shape is beneficial to the yield of rice. Molecular understanding of the leaf primordia and polarity establishment plays a significant role in exploring the genetic regulatory network of leaf morphogenesis. In recent years, researchers have cloned an array of coding genes and a few non-coding small RNAs involved in rice leaf development through regulating the development of leaf primordia, vascular bundles, sclerenchyma cells, bulliform cells, cell walls and epidermis cells. These genes and their interactions play critical roles in rice leaf development through the determination and regulatory role in gene expression, and their coordination with other genetic networks or signal pathways. But the relationship among these genes is poorly defined and the underlying network is still unclear. In this review, we introduced the regulatory pathways of leaf primordium development and leaf polarity establishment, mainly the relationship between cell development mechanism and leaf polarity establishment, focusing on how leaf tissue affects leaf shape. Hopefully, the regulation network reviewed here has immediate implications for future research and genomic design breeding. Key words: rice; leaf morphogenesis; molecular mechanism; tissue cell; leaf polarity establishment Leaf is the determinate organ that serves as a main The normal development of leaf tissue is essencial photosynthetic structure of plants (Piazza et al, 2005). to the maintenance of leaf morphology, which differs Leaf architecture is closely related to environmental across species (Hasson et al, 2010). Rice leaves have factors such as light intensity, temperature and humidity, the typical characteristics of monocotyledonous leaves which influences plant transpiration, stress resistance, with no palisade tissues or sponge tissues in mesophyll photosynthetic efficiency and other physiological cells and no known difference in the distribution of characteristics (Mishra and Panda, 2017; Liu et al, stomata between the upper and lower epidermis. The 2018; Zhang et al, 2018; Chen T et al, 2019). Lamina normal developments of vascular bundles, bulliform posture is an important agronomic trait closely associated cells, sclerenchyma cells, epidermal cells, stomata and with plant type. The regulation of leaf posture is cell walls form the premise for the maintenance of the considered as an effective means to improve crop yield. isobilateral leaf of rice. In recent years, many genes or Leaf development includes primordium initiation, quantitative trait locus (QTLs) related to leaf morpho- tissue differentiation, polarity establishment, leaf extension genesis have been cloned. They are involved in the and maturation. Adaxial-abaxial leaf polarity, proximal- signaling pathways of phytohormone, transcription distal leaf polarity, and median-lateral leaf polarity factors, microRNAs, and regulates leaf shape through form a three-dimensional axial polarity that directly the division and differentiation of cells in leaf. determines leaf morphology (Itoh et al, 2008). Furthermore, the abnormal developments of vascular Received: 25 December 2019; Accepted: 9 May 2020 Corresponding authors: ZHANG Guangheng ([email protected]); QIAN Qian ([email protected]) Copyright © 2020, China National Rice Research Institute. Hosting by Elsevier B V This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) Peer review under responsibility of China National Rice Research Institute http://dx.doi.org/10.1016/j.rsci.2020.09.004 (C skelaton, Osmotic regulation, N storage, Insect Deterrant) 2 . WANG Jiajia, et al. How Histiocytes Modulate Leaf Polarity Establishment 469 bundles, sclerenchyma cells, bulliform cells, epidermis cells (Ito et al, 2001). Furthermore, studies have and cell walls also lead to the alterment of leaf shown that the expression of KNOX is positively architecture (Fig. 1). This paper provided an overview regulated by cytokinin and KNOX itself. The positive of the relationship between cell development and leaf self-regulation of OSH1 is essential for the shape, with an emphasis on leaf polarity and leaf maintenance of the rice apical meristem (Tsuda et al, primordium development, which may contribute to the 2011). Further studies have shown that OSH1 inhibits understanding of leaf morphogenesis mechanism at the brassinosteroid (BR) pathway by activating its cellular level, and provide foundation for the further catabolic gene, thereby controlling the establishment elucidation of leaf morphogenesis mechanisms. and maintenance of SAM (Tsuda et al, 2014). Another member of the rice KNOX family class I gene, Leaf primordium development affects OSH71/Oskn2, interacts with the growth regulator rice leaf polarity establishment OsGRF3, which acts as a transcriptional repressor involved in the regulation of Oskn2-mediated SAM Shoot apical meristem (SAM) is at the top of the stem formation (Postma-Haarsma et al, 1999; Kuijt et al, and forms the birthplace of both leaves and stems. The 2014). Long-chain fatty acid ω-alcohol dehydrogenase initiation and maintenance of SAM are required for ONI3 inhibits the expression of KNOX (Akiba et al, the continuous development of the stem (Hasson et al, 2014), which in turn inhibits the accumulation of 2010). As a major phytohormone, auxin precisely auxin and regulates the growth and development of regulates the primordium differentiation of SAM rice shoots (Fang et al, 2015). The mutual antagonism (Guenot et al, 2012), and induces differentiation of of KNOX I and the MYB family ASYMETRIC organ primordium during the early stages of leaf LEAVES1/ROUGH SHEATH2/PHANTASTICA (ARP) development (Kalve et al, 2014). High concentrations proteins in Arabidopsis are key to the initiation of leaf of auxin inhibit the activity of KNOTTED-like primordia. ARP inhibits the activity of KNOX at the homebox 1 (KNOX1) (Su et al, 2011), which positively primordium, whilst KNOX is highly expressed in all regulates the biosynthesis of cytokinin and negatively meristematic tissues outside the primordial start site regulates the synthesis of gibberellin (GA) through (Byrne et al, 2000, 2002). inhibiting the activity of GA20ox (Kalve et al, 2014). Normal initiation of the leaf is essential to morphogenesis of late leaves. Phyllotaxy and Members of the KNOX gene family have important plastochron form the basis of plant architecture regulatory roles in the initiation of leaf primordia and the (Miyoshi et al, 2004). The plastochron genes PLA1 correct establishment of the leaf apical axis (Hay and and PLA2 mediate leaf maturation and the temporal Tsiantis, 2009). Rice KNOX family class I gene OSH1 pattern of successive leaf initiation (Mimura and Itoh, is expressed prior to organ differentiation in specific 2014). PLA1 encodes cytochrome P450 CYP78A11, regions during early embryogenesis (Sato et al, 1996). and affects initial development of leaves and The class I homeodomain gene of the KNOX family termination of vegetative growth (Miyoshi et al, 2004). plays an important role in the formation and PLA2/LHD2 encodes an RNA-binding protein that maintenance of the undetermined meristematic state of regulates rice shoot development through KNOX and hormone-related genes (Xiong et al, 2006). PLA1 and PLA2 play a key role in the downstream of gibberellin (GA) signaling pathway and regulate leaf maturation (Mimura et al, 2012). PLA3/GO encodes a glutamate carboxypeptidase II, which is expressed in the whole plant body and can catabolize small peptides, regulating various signaling pathways involved in a number of processes. The loss-of-function mutant of PLA3 shows similar phenotypes to pla1 and pla2. Furthermore, pla3 shows pleiotropic phenotypes, including enlarged embryo, seed vivipary, defects in Fig. 1. Overview of tranverse section of rice leaf. BC, Bulliform cell; LV, Large vascular bundle; SV, Small vascular SAM maintenance and abnormal leaf morphology bundle; SC(ad), Sclerenchyma cell (adaxial); SC(ab), Sclerenchyma (Kawakatsu et al, 2009). Though the regulatory cell (abaxial). mechanism of early initiation of leaf primordia has 470 Rice Science, Vol. 27, No. 6, 2020 Adaxial domain Abaxial domain A Initiation of leaf Establishment and B primordia maintenance of SAM miR165/166 AGO1 ZPR CK BR signal pathway ONI3 KANADI IPT7 AUX1 HD-ZIP III ARP KNOX1 Auxin maximum PIN1 ARP (AS1/AS2) YABBY WOX3 GA 2ox GA20-ox GRF3 GA3ox2 Maintain the meristem in an tasiRNA ARF3/4 GA undifferentiated state Fig. 2. Genetic and molecular network controlling initiation of leaf primordia (A) and adaxial-abaxial leaf polarity (B). ↑ indicates acceleration; indicates inhibition. been clearly defined (Fig. 2-A), the regulatory role of class III gene, OSHB4, regulates leaf development in different tissue structures in the establishment of leaf an auxin-dependent manner in rice (Li Y Y et al, 2016). polarity is not well understood. miRNA165/166 regulates the adaxial-abaxial polarity of leaves by inhibiting the HD-ZIP class III gene Tissue structure regulates rice leaf polarity (Zhang et al, 2018). Moreover,
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