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. 2023 Dec 7:14:1293424.
doi: 10.3389/fpls.2023.1293424. eCollection 2023.

Overview of molecular mechanisms of plant leaf development: a systematic review

Zhuo Lv  1   2   3 , Wanqi Zhao  1   2   3 , Shuxin Kong  1   2   3 , Long Li  1   2   3 , Shuyan Lin  1   2   3
Affiliations

Overview of molecular mechanisms of plant leaf development: a systematic review

Zhuo Lv et al. Front Plant Sci. .

Abstract

Leaf growth initiates in the peripheral region of the meristem at the apex of the stem, eventually forming flat structures. Leaves are pivotal organs in plants, serving as the primary sites for photosynthesis, respiration, and transpiration. Their development is intricately governed by complex regulatory networks. Leaf development encompasses five processes: the leaf primordium initiation, the leaf polarity establishment, leaf size expansion, shaping of leaf, and leaf senescence. The leaf primordia starts from the side of the growth cone at the apex of the stem. Under the precise regulation of a series of genes, the leaf primordia establishes adaxial-abaxial axes, proximal-distal axes and medio-lateral axes polarity, guides the primordia cells to divide and differentiate in a specific direction, and finally develops into leaves of a certain shape and size. Leaf senescence is a kind of programmed cell death that occurs in plants, and as it is the last stage of leaf development. Each of these processes is meticulously coordinated through the intricate interplay among transcriptional regulatory factors, microRNAs, and plant hormones. This review is dedicated to examining the regulatory influences of major regulatory factors and plant hormones on these five developmental aspects of leaves.

Keywords: leaf polarity; leaf primordium; leaf senescence; leaf shape; leaf size.

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Conflict of interest statement

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

Figures

Figure 1
Figure 1
Initiation of leaf primordium. SAM is divided into three functional regions [central region (CZ), peripheral region (PZ) and costal region (OC)] and Layer1 (L1), Layer2 (L2) and Layer3(L3). WUS activates CLV3, and CLV3 further binds to CLV1/2, thereby inhibiting WUS expression. Auxin accumulation in the flanks of SAM through PIN1/AUX1 mediated polar transport triggers primordium development. In addition, KNOX1 maintains the role of stem cells, positively regulates CK, negatively regulates GA signaling through IPT7 and GA20ox, and ARF regulates the emergence of young primordiae (→ represents positive regulation, and T-shaped arrows represent negative regulation. The same below.) (Barkoulas et al., 2007; Bar and Ori, 2014; Kalve et al., 2014; Wang et al., 2021a).
Figure 2
Figure 2
Establishment of leaf polarity. The developing leaf primordium has three domains, and the transcription factors in the three domains inhibit each other’s expression and control each other. Transcripts of AS1/AS2, HD-ZIPIII and tasi-ARF accumulate in the adaxial domain of the leaf primordium, transcripts of ARF 3/ARF4, KAN and miR165/166 accumulate in the abaxia domain, and WOX1/PRS are expressed in the intermediate domain of the leaf primordium. AGO10 inhibits miR165/166, AGO1 regulates miR165/166 and miR165/166 inhibits HD-ZIPIII. AGO7 stabilizes ta-siR-ARF, and ta-siR-ARF degrades of ARF2/3/4. tasi-ARF and miR165/166 Rnas can move between cells and inhibit ARF2/3/4 and HD-ZIPIII after transcription, and ARF2/3/4 is controlled by auxin. KAN and HD-ZIPIII antagonized each other, and ARF2/3/4 and KAN were inhibited by AS1/AS2. KAN inhibited the expression of WOX1 and PRS, while WOX1 and PRS inhibited the expression of KAN. Adaxial expression of MP and off-axes enrichment of auxin together localized WOX1 and PRS expression in the intermediate domain. In addition, MP may be the direct target of positively expressed HD-ZIPIII, and YAB promotes the expression of WOX1/PRS with KAN and ARF2/3/4, while YAB promotes the expression of WOX1/PRS (Barkoulas et al., 2007; Kalve et al., 2014; Du et al., 2018; Wang et al., 2021a).
Figure 3
Figure 3
Regulation of leaf size (A case study of Arabidopsis leaves). Leaf size is controlled by cell proliferation and cell expansion. ARGOS promotes cell proliferation through ANT and CYCD3, and miR319 negatively regulates TCP and GRF/GIF transcription factors to promote proliferation. TOR and ARL promote cell expansion, TCP activates the NGA to promote cell expansion, BB and DA1 control the timing of proliferation, and abscisic acid partially facilitates the transition by regulating DA1. KLUH, SWP and CK promote cell proliferation, ORS1, GA and BR have positive effects on cell proliferation and cell expansion (Barkoulas et al., 2007; Kalve et al., 2014; Du et al., 2018; Wang et al., 2021a).
Figure 4
Figure 4
Leaf edge development (taking Arabidopsis leaf as an example). During leaf margin development, miRNA164 and CUC2 are expressed in the overlapping regions of serrated sagging, CUC2 promotes the establishment of PIN1 convergence points, and PIN1 convergence points produce the maximum value of auxin along the serrated tip of leaf margin. Auxin maximously inhibits CUC2 at the tip of the tooth and promotes the growth of the tooth (Barkoulas et al., 2007; Wang et al., 2021a).
Figure 5
Figure 5
Hormonal and gene regulation of leaf senescence. YCCA6 regulates auxin biosynthesis and inhibits leaf senescence. The AP2/ERF transcription factor CRF6 mediated by cytokinin inhibits senescence, and the cytokinin receptor AHK3 regulates leaf senescence through the regulatory factor ARR2. The abnormal accumulation of DELLA protein delayed leaf senescence by blocking GA biosynthesis. Ethylene activated AP2/ERF gene to regulate leaf senescence, ERF transcription factor inhibited the expression of ESP/ESR, a negative regulator of leaf senescence, ESR knockout promoted leaf senescence, while ESR overexpression did the opposite. EIN3 activates ORE1 and NAP to positively regulate leaf senescence. EIN3 inhibits miR164 transcription and up-regulates the transcription level of ORE1/NAC2, the target gene of miR164. ABA induces WRKY transcription factor and promotes early senescence of leaves under dark treatment. SA treatment induces SAGs expression, and WRKY influences plant aging and defense signaling pathways in SA-mediated signaling cascades. WRKY interacts with JA biosynthesis gene LOX3 to promote leaf senescence, MYC2/3/4 protein can activate JA-induced chlorophyll degradation, and the signaling pathway of MYC2/3/4 and NAC protein ANAC019/055/072 induces leaf senescence. BRs activates BZR family transcription factors to promote leaf senescence. SL genes MAX3 and MAX4 accelerate leaf senescence (Mayta et al., 2019; Guo et al., 2021a).
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The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Key Research & Development Program of China (2021YFD2200503); the National Natural Science Foundation of China (32371977). We also appreciate all the authors for their valuable works.
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