Tree Genetics and Molecular Breeding 2024, Vol.14 http://genbreedpublisher.com/index.php/tgmb © 2024 GenBreed Publisher, registered at the publishing platform that is operated by Sophia Publishing Group, founded in British Columbia of Canada. All Rights Reserved.
Tree Genetics and Molecular Breeding 2024, Vol.14 http://genbreedpublisher.com/index.php/tgmb © 2024 GenBreed Publisher, registered at the publishing platform that is operated by Sophia Publishing Group, founded in British Columbia of Canada. All Rights Reserved. GenBreed Publisher is an international Open Access publisher specializing in tree genetics and molecular breeding, trees genetic diversity and conservation genetics registered at the publishing platform that is operated by Sophia Publishing Group (SPG), founded in British Columbia of Canada. Publisher GenBreed Publisher Editedby Editorial Team of Tree Genetics and Molecular Breeding Email: edit@tgmb.genbreedpublisher.com Website: http://genbreedpublisher.com/index.php/tgmb Address: 11388 Stevenston Hwy, PO Box 96016, Richmond, V7A 5J5, British Columbia Canada Tree Genetics and Molecular Breeding (ISSN 1927-5781) is an open access, peer reviewed journal published online by GenBreed Publisher. The journal publishes all the latest and outstanding research articles, letters and reviews in all aspects of tree genetics and molecular breeding, include studies in tree genetics and molecular breeding, include studies in crop/fruit/forest/ornamental/horticultural trees genetic diversity, conservation genetics, molecular genetics, evolutionary genetics, population genetics, physiology, biochemistry, transgene, genetic rule analysis, QTL analysis, vitro propagation; fruit/forest/ornamental/horticultural trees breeding studies and advanced breeding technologies. All the articles published in Tree Genetics and Molecular Breeding are Open Access, and are distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. GenBreed Publisher uses CrossCheck service to identify academic plagiarism through the world’s leading plagiarism prevention tool, iParadigms, and to protect the original authors’ copyrights.
Tree Genetics and Molecular Breeding (online), 2024, Vol. 14 ISSN 1927-5781 http://genbreedpublisher.com/index.php/tgmb © 2024 GenBreed Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher Latest Content Molecular Mechanisms of Cambium Formation and Activity Maintenance: A Systematic Review of the Collaborative Regulation of Tree Stem Cells in Growth, Development, and Environmental Adaptation Yongquan Lu, Yixuan He, Xuze Wang, Faustin Mutudi Tshibunga Tree Genetics and Molecular Breeding, 2024, Vol. 14, No. 5, 218-228 The Role of Canopy Management in Optimizing Grapevine Yield and Quality Kaiwen Liang Tree Genetics and Molecular Breeding, 2024, Vol. 14, No. 5, 229-238 Advances in Molecular Breeding Techniques for Pitaya (Hylocereus) Dandan Huang, Zhen Li Tree Genetics and Molecular Breeding, 2024, Vol. 14, No. 5, 239-246 Application Potential and Technical Challenges of Agave in Bioethanol Production Wenying Hong, Wenzhong Huang Tree Genetics and Molecular Breeding, 2024, Vol. 14, No. 5, 247-255 Ecological Factors Influencing Tea Yield: A Comprehensive Review Yufen Wang, Chunyu Li, Xiaocheng Wang Tree Genetics and Molecular Breeding, 2024, Vol. 14, No. 5, 256-268
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 218-228 http://genbreedpublisher.com/index.php/tgmb 218 Systematic Review Open Access Molecular Mechanisms of Cambium Formation and Activity Maintenance: A Systematic Review of the Collaborative Regulation of Tree Stem Cells in Growth, Development, and Environmental Adaptation Yongquan Lu , Yixuan He, Xuze Wang, Faustin Mutudi Tshibunga State Key Laboratory of Subtropical Silviculture, College of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou, 311300, Zhejiang, China Corresponding email: luyongquan@zafu.edu.cn Tree Genetics and Molecular Breeding, 2024, Vol.14, No.5 doi: 10.5376/tgmb.2024.14.0021 Received: 08 Aug., 2024 Accepted: 13 Sep., 2024 Published: 21 Sep., 2024 Copyright © 2024 Lu et al., This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Lu Y.Q., He Y.X., Wang Z.X., and Tshibunga F.M., 2024, Molecular mechanisms of cambium formation and activity maintenance: a systematic review of the collaborative regulation of tree stem cells in growth, development, and environmental adaptation, Tree Genetics and Molecular Breeding, 14(5): 218-228 (doi: 10.5376/tgmb.2024.14.0021) Abstract Seasonal changes and environmental conditions, especially temperature, significantly affect cambium activation and wood formation, affecting tree growth and adaptation. Advanced genetic and epigenome analyses have revealed the importance of DNA methylation and miRNA in regulating cambium activity. The synergistic regulation of cambium activity involves a multifaceted network of genetic, hormonal, and environmental interactions, and understanding these mechanisms provides valuable insights into tree growth and development, with important implications for forestry management and climate change adaptation. This study synthesizes findings from a variety of related studies highlighting the complex interplay of genetic, hormonal, and environmental factors in cambium regulation. Through the identification of specific genes and signaling pathways regulating auxin homeostasis such as MADS-box genes VCM1 and VCM2, the molecular regulation of secondary growth was further clarified. The aim of this study was to elucidate the molecular mechanisms of cambium formation and activity maintenance in trees, focusing on the synergistic regulation of tree stem cells in growth, development and environmental adaptation. Keywords Cambium; Secondary growth; Phytohormones; Gene regulation; Environmental adaptation 1 Introduction The cambium is a critical meristematic tissue in trees responsible for secondary growth, which leads to the thickening of stems and roots. This tissue is composed of stem cells that divide to produce secondary xylem (wood) and secondary phloem (bast) (Fischer et al., 2019; Turley and Etchells, 2021). The cambium's activity is essential for the formation of wood, which constitutes a significant portion of the world's biomass (Turley and Etchells, 2021). The regulation of cambial growth involves complex interactions between genetic, hormonal, and environmental factors (Savidge, 2001; Groover and Robischon, 2006; Ursache et al., 2013). Understanding these mechanisms is crucial for comprehending how trees grow, develop, and adapt to their environments. Studying cambium formation and activity maintenance is vital for several reasons. Firstly, it provides insights into the fundamental processes of plant growth and development, particularly in woody plants (Groover and Robischon, 2006; Turley and Etchells, 2021). Secondly, the cambium's role in wood production has significant ecological and economic implications, as wood is a major renewable resource (Etchells et al., 2015; Turley and Etchells, 2021). Additionally, understanding how environmental factors such as temperature and seasonal changes influence cambial activity can help predict and mitigate the impacts of climate change on forest ecosystems (Begum et al., 2013; Chen et al., 2021). Moreover, advances in genetic and molecular research on cambium regulation can lead to improved tree breeding and biotechnology applications, enhancing wood production and quality (Agustí et al., 2011; Etchells et al., 2015). This study elucidates the molecular mechanisms underlying cambium formation and activity maintenance in trees, which includes exploring the genetic, hormonal, and environmental factors that regulate cambial stem cell dynamics and secondary growth. By synthesizing current knowledge and recent discoveries, this study aims to provide a comprehensive understanding of the collaborative regulation of tree stem cells in growth, development, and environmental adaptation and discusses potential areas for future research and applications in forestry and biotechnology.
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 218-228 http://genbreedpublisher.com/index.php/tgmb 219 2 Identification and Functional Analysis of Cambium-Specific Expression Genes 2.1 Methods for identifying cambium-specific genes The identification of cambium-specific genes has been facilitated by various advanced techniques. One notable method involves the use of laser capture microdissection combined with transcriptome profiling, which allows for the precise isolation and analysis of cambium tissues. This approach was effectively utilized to identify genes induced during different phases of cambium formation in Arabidopsis thaliana (Agustí et al., 2011). Additionally, the use of in vitro systems to induce cambium formation in isolated stem fragments has proven valuable in characterizing transcriptome remodeling in a tissue- and stage-specific manner (Agustí et al., 2011). In coniferous trees, such as Pinus sylvestris, the expression profiles of cambium-specific genes were studied by collecting trunk tissue samples at different stages of ontogenesis and cambial growth. This method enabled the identification of spatial and temporal expression patterns of key regulatory genes (Galibina et al., 2023). Furthermore, comprehensive analyses of transcriptome profiles, DNA methylome, and miRNAs during the transition from dormancy to activation in Populus tomentosa have provided insights into the molecular mechanisms underlying cambium activity (Chen et al., 2021). 2.2 Functional roles of identified genes The functional roles of identified cambium-specific genes are diverse and critical for the regulation of cambium activity and secondary growth. For instance, the receptor-like kinases REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1) have been identified as opposing regulators of cambium activity in Arabidopsis, with RUL1 inhibiting and MOL1 promoting lateral growth (Agustí et al., 2011). In Populus, two MADS-box genes, VCM1 andVCM2, were found to modulate auxin homeostasis, thereby regulating vascular cambium proliferation and secondary growth (Zheng et al., 2020; Haas et al., 2022). The WUSCHEL-RELATED HOMEOBOX (WOX) gene family, particularly WOX4, plays a crucial role in maintaining and proliferating stem cells in the cambium. In Scots pine, the expression of WOX4 was highest during active cell proliferation in the cambial zone, indicating its importance in cambial activity (Galibina et al., 2023). Similarly, in Populus, WOX4-like genes were shown to control cell division activity in the vascular cambium, with their expression regulated byCLE41-related genes (Kucukoglu et al., 2017). 2.3 Comparative analysis of cambium-specific genes across different tree species Comparative analysis of cambium-specific genes across different tree species reveals both conserved and species-specific regulatory mechanisms. For example, the CLE41/44-PXY-WOX signaling module, which regulates cambial growth in Scots pine, is also conserved in Populus, where it controls cell division activity in the vascular cambium (Kucukoglu et al., 2017; Galibina et al., 2023). This suggests an evolutionarily conserved program for the regulation of vascular cambium activity between angiosperm and gymnosperm tree species (Wang, 2020). In addition, the identification of stress-response transcription factors that control cambium activity in radish and their comparison with Arabidopsis data highlights the conservation of gene-regulatory networks that integrate environmental sensing and growth (Hoang et al., 2020; Furuya et al., 2021). The role of miRNAs and DNA methylation in regulating cambium activity in Populus further underscores the complexity and diversity of epigenomic regulation across different species (Chen et al., 2021). These studies provide valuable insights into the molecular mechanisms of cambium formation and activity maintenance, highlighting the collaborative regulation of tree stem cells in growth, development, and environmental adaptation. 3 Regulatory Mechanisms of Hormones in Cambium Formation and Activity Maintenance 3.1 Overview of hormone regulation in plant stem cells Hormones play a crucial role in the regulation of plant stem cells, particularly in the cambium, which is responsible for secondary growth. The cambium’s activity is influenced by a complex interplay of hormonal signals, including auxin, cytokinin, gibberellin, and strigolactones, among others. These hormones coordinate to regulate the balance between cell proliferation and differentiation, ensuring the proper formation and maintenance of the cambium (Groover and Robischon, 2006; Turley and Etchells, 2021; Ben-Targem et al., 2021; Hu et al., 2021).
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 218-228 http://genbreedpublisher.com/index.php/tgmb 220 3.2 Cytokinin regulation 3.2.1 Pathway components Cytokinins are a class of plant hormones that promote cell division and differentiation. Key components of the cytokinin signaling pathway include cytokinin receptors (such as AHKs), histidine phosphotransfer proteins (AHPs), and response regulators (ARRs). These components work together to mediate the effects of cytokinins on cambial activity (Elo et al., 2009; Oles et al., 2017). 3.2.2 Role in cambium formation Cytokinins are essential for the initiation of cambium formation. They promote the proliferation of cambial stem cells and the establishment of the cambial zone. Studies have shown that cytokinin signaling is crucial for the early stages of cambium development, facilitating the transition from primary to secondary growth (Groover and Robischon, 2006; Turley and Etchells, 2021). 3.2.3 Role in cambium activity maintenance In addition to their role in cambium formation, cytokinins are also vital for maintaining cambial activity. They help sustain the division of cambial cells and the production of secondary xylem and phloem. The balance between cytokinin and auxin signaling is particularly important for the continuous activity of the cambium, as these hormones often have antagonistic effects (Oles et al., 2017; Ben-Targem et al., 2021). 3.3 Auxin regulation 3.3.1 Pathway components Auxins are another critical group of plant hormones involved in cambium regulation. The auxin signaling pathway includes auxin receptors (such as TIR1/AFB), Aux/IAA proteins, and ARF transcription factors. These components interact to modulate gene expression in response to auxin levels, influencing cambial activity (Oles et al., 2017; Turley and Etchells, 2021; Hu et al., 2021). 3.3.2 Role in cambium formation Auxins play a pivotal role in the formation of the cambium by promoting the differentiation of procambial cells into cambial stem cells. High auxin concentrations are typically found in regions where cambium formation is actively occurring, indicating its importance in initiating secondary growth (Groover and Robischon, 2006; Elo et al., 2009; Turley and Etchells, 2021). 3.3.3 Role in cambium activity maintenance Auxins are also crucial for the maintenance of cambial activity. They regulate the balance between cell division and differentiation within the cambium, ensuring a steady supply of new cells for secondary xylem and phloem production. Auxin gradients within the plant tissue help direct the pattern of cambial growth and activity (Oles et al., 2017; Ben-Targem et al., 2021; Hu et al., 2021). In summary, the regulation of cambium formation and activity by hormones such as cytokinins and auxins is a complex and finely tuned process. These hormones interact with each other and with other signaling pathways to ensure the proper development and maintenance of the cambium, which is essential for the secondary growth of plants. Understanding these regulatory mechanisms provides valuable insights into plant development and has potential applications in forestry and agriculture (Groover and Robischon, 2006; Elo et al., 2009; Oles et al., 2017; Turley and Etchells, 2021; Ben-Targem et al., 2021; Hu et al., 2021). 4 Adaptive Response Mechanisms of Cambium Stem Cells Under Environmental Stress Conditions 4.1 Types of environmental stress affecting cambium Cambium stem cells in trees are subjected to various environmental stressors that can significantly impact their activity and function. These stressors include abiotic factors such as temperature fluctuations, drought, and nutrient availability, as well as biotic factors like pathogen attacks and herbivory. Temperature, in particular, plays a crucial role in the timing of cambial reactivation and xylem differentiation. Elevated temperatures from late
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 218-228 http://genbreedpublisher.com/index.php/tgmb 221 winter to early spring can lead to earlier initiation of cambial activity, extending the growth period but also increasing the risk of frost damage due to decreased cold tolerance post-reactivation (Begum et al., 2013). Additionally, the immediate environment of cambial cells, including weather and nutritional factors, continuously varies, influencing wood formation and the variability in wood properties (Downes et al., 2009). 4.2 Molecular response mechanisms to abiotic stress Cambium stem cells employ various molecular mechanisms to respond to abiotic stress. For instance, temperature-induced changes in the stability of microtubules are crucial for the reactivation of cambial cells and subsequent xylem differentiation (Begum et al., 2013). Hormones, peptides, and mechanical cues are also believed to orchestrate the response of cambial activity to environmental factors, although the exact mechanisms remain to be fully uncovered (Fischer et al., 2019). In Populus, the peptide PtrCLE20 has been identified as a repressor of vascular cambium activity, suggesting a role in modulating growth in response to environmental cues (Zhu et al., 2019). Furthermore, conserved gene-regulatory networks involving stress-response transcription factors, such as ERF-1, integrate environmental sensing with cambium-driven growth, highlighting the complex interplay between environmental signals and cambial activity (Chiatante et al., 2018; Hoang et al., 2020). 4.3 Molecular response mechanisms to biotic stress In response to biotic stress, such as pathogen attacks, cambium stem cells activate specific molecular pathways to mitigate damage and maintain growth. The identification of receptor-like kinases, such as REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), which act as opposing regulators of cambium activity, underscores the importance of cell-to-cell communication in the cambium's response to biotic stress (Agustí et al., 2011). These signaling components help coordinate the cambium's activity, ensuring the production of secondary phloem and xylem even under stress conditions. Additionally, the dynamic nature of cambial stem cell activity, influenced by mobile signals and intercellular communication, plays a critical role in the plant's ability to adapt to biotic stress (Bhalerao and Fischer, 2017; Fischer et al., 2019). 4.4 Integration of stress signals in cambium regulation The integration of stress signals in cambium regulation involves a complex network of molecular interactions. Phytohormones, transcription factors, and peptide-receptor modules are key players in this process. Recent studies have highlighted the roles of mobile transcription factors and intercellular signaling in the regulation of cambium activity, emphasizing the crosstalk between different regulatory pathways (Turley and Etchells, 2021). The environment of cambial cells, including fluxes in phytohormones, carbohydrates, and physical factors, influences gene expression and enzyme kinetics, thereby modulating cambial activity in response to stress (Savidge, 2001). Understanding these integrative mechanisms is crucial for developing strategies to enhance tree growth and resilience under changing environmental conditions. 5 Collaborative Regulation Networks of Cambium, Xylem, and Phloem Development 5.1 Gene networks involved in cambium development The development and activity of the vascular cambium are regulated by complex gene networks. Key transcription factors such as WUSCHEL-RELATED HOMEOBOX 4 (WOX4) and KNOTTED-like from Arabidopsis thaliana 1 (KNAT1) play crucial roles in cambium development. Mutations in these genes can lead to significant changes in cambial activity, highlighting their importance in the regulatory network (Zhang et al., 2019). Additionally, MADS-box genes like VCM1 and VCM2 have been identified to modulate auxin homeostasis, which is essential for cambium proliferation and secondary growth in Populus (Zheng et al., 2020). The interaction between these genes and hormonal pathways, such as auxin and gibberellin signaling, further underscores the complexity of the gene networks involved in cambium development (Ben-Targem et al., 2021). 5.2 Interactions between cambium, xylem, and phloem gene networks The gene networks regulating cambium activity are intricately linked with those controlling xylem and phloem development. For instance, the transcription factors WOX4 and SHORT VEGETATIVE PHASE (SVP) have dual roles in cambial cell proliferation and xylem differentiation (Zhang et al., 2019). Hormonal signaling pathways, including auxin and gibberellin, also play a pivotal role in coordinating the development of these tissues. Auxin
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 218-228 http://genbreedpublisher.com/index.php/tgmb 222 gradients across the cambium area are crucial for regulating the differentiation of cambial derivatives into xylem and phloem (Zheng et al., 2020). Moreover, the interaction between auxin and gibberellin signaling pathways has been shown to promote xylem expansion and maintain cambium homeostasis (Ben-Targem et al., 2021). The dual regulation of xylem formation by the PaC3H17-PaMYB199 module in Populus further exemplifies the collaborative regulation of these gene networks (Tang et al., 2019). 5.3 Case studies of collaborative regulation in specific tree species In Populus, the MADS-box genes VCM1 andVCM2 have been shown to regulate cambium activity and secondary growth by modulating auxin homeostasis (Figure 1). Knock-down of these genes enhances cambium proliferation and xylem differentiation, while their overexpression suppresses these processes (Zheng et al., 2020). Another study in Populus identified the PaC3H17-PaMYB199 module, which regulates xylem formation through an auxin-mediated pathway. This module controls cambial cell proliferation and secondary cell wall thickening, highlighting the complex regulatory networks involved in wood formation (Figure 2) (Tang et al., 2019). Figure 1VCM1and VCM2expression and phenotypes of their transgenic lines (Adopted from Zheng et al., 2020) Image caption: (A and B) qRT-PCR analysis of VCM1 (A) andVCM2 (B) expression in different tissues. Values are means ± SD (n = 3 biological replicates). SMT, shoot meristem tissue; YL, young leaf; IN, internode; YT, young roots. (C and D) GUS activity in transgenic Populus driven by the VCM1 promoter (C) and the VCM2 promoter (D). Ca, cambium; Xy, xylem; Ph, phloem. Scale bar corresponds to 100 μm. (E) Phenotypes of the wild-type (WT), VCM1 and VCM2 knock-down lines, (DR4 and DR15) and VCM1 overexpression lines (UR13 and UR25). Scale bar corresponds to 10 cm. (F) qRT-PCR analysis of VCM1 and VCM2 expression in transgenics. Values are means ± SD (n = 3 biological replicates). (G–I) Cross-section of the 13th internode stained with toluidine blue (above) and enlarged rectangle area (below). (G) WT; (H) VCM1 and VCM2 knock-down lines; (I), VCM1 overexpression lines. Xy, xylem; Ph, phloem; Ca, cambium. Scale bars correspond to 200 μm (50 μm in enlargements). (J) Number of cambium cell layers (n> 50). (K) Number of xylem cell layers (n > 50). Plants used for analysis were grown in a phytotron for 3 months. Values are means ± SD. Statistical significance of differences was calculated based on two-tailed, two-sample Student's t-test (**P < 0.01, *P < 0.05) (Adopted from Zheng et al., 2020)
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 218-228 http://genbreedpublisher.com/index.php/tgmb 223 Figure 2PaMYB199 interacts withPaC3H17 (Adopted from Tang et al., 2019) Image caption: (a) Yeast two hybrid assays were performed using PaMYB199 fused to the DNA binding domain (BD) and PaC3H17 fused to the activation domain (AD). AH109 cells containing different plasmid combinations were grown on selective medium SD-LTHA (L, leucine; T, tryptophan; H, histidine; A, adenine) with 0 or 20 mM 3-amino-1,2,4-triazole, and stained for α-galactosidase activity. (b) In vitropull-down assays. GST-PaC3H17 and MBP-PaMYB199 proteins were immunoprecipitated with an anti-GST antibody and then immunoblotted using an anti-MBP antibody. (c) Bimolecular fluorescence complementation assay showing that PaC3H17-YFPNE and PaMYB199-YFPCE interact to form a functional yellow fluorescent protein (YFP) in the nucleus of Arabidopsis leaf protoplasts. The DNA fluorochrome 4′,6-diamidino-2-phenylindole (DAPI) was used to stain the cell nucleus (blue). Bars, 10 μm. (d) Co-immunoprecipitation assay. 35S:FLAG-PaC3H17 (GFP-FLAGas the control) and 35S:PaMYB199-HA were co-transformed into Arabidopsis leaf protoplasts. Total proteins were immunoprecipitated using an anti-HA antibody and the immunoblots were probed with an anti-FLAG antibody (Adopted from Tang et al., 2019) In Arabidopsis, the transcription factors WOX4 and KNAT1 are central to cambium development. Their interaction with other regulatory pathways, such as those involving phytohormones like auxin and cytokinin, underscores the collaborative nature of these gene networks (Zhang et al., 2019). Additionally, the role of DELLA proteins in mediating gibberellin signaling and their interaction with AUXIN RESPONSE FACTORS (ARF6 and ARF8) further illustrates the intricate regulation of cambium and xylem development (Figure 3) (Ben-Targem et al., 2021). In Betula pendula, trunk girdling experiments have shown that changes in photoassimilate levels can significantly impact cambium activity and the differentiation of xylem and phloem. Increased photoassimilates lead to enhanced phloem formation and changes in the anatomical structure of the conducting tissues, demonstrating the environmental regulation of cambium activity (Serkova et al., 2022). 6 Applications and Prospects of Gene Editing Technology in Cambium Regulation 6.1 Overview of gene editing technologies Gene editing technologies, such as CRISPR-Cas9, have revolutionized the field of plant biology by enabling precise modifications of specific genes. These technologies allow for targeted alterations in the genome,
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 218-228 http://genbreedpublisher.com/index.php/tgmb 224 facilitating the study and manipulation of gene functions in various biological processes, including cambium regulation. CRISPR-Cas9, in particular, has been widely adopted due to its simplicity, efficiency, and versatility in editing genes across different species (Shen et al., 2021). Figure 3 ARF6 and ARF8 expression pattern overlaps with RGA and GAI during hypocotyl secondary growth (Adopted from Ben-Targem et al., 2021) Image caption: (A–D) Hypocotyl vibratome cross-sections at 0, 8 and 20 d after flowering (daf). Left and middle panels: confocal images of sections cleared with ClearSee and stained with Calcofluor White showing GFP signal in the nuclei (red arrows). Right panels: GUS assay on vibratome sections stained with phloroglucinol (red arrows indicates the phloem). (A) RGA:NLS-GFP-GUS (left and middle panels) and RGA:GUS (right panel). (B) GAI:NLS-GFP-GUS (left and middle panels) and GAI:GUS (right panel). (C) ARF6:NLS-3xGFP (left and middle panels) and ARF6:GUS (right panel). (D) ARF8:NLS-3xGFP (left and middle panels) and ARF8:GUS (right panel). White scale bar: 20 μm and black scale bars: 20 μm (Adopted from Ben-Targem et al., 2021) 6.2 Applications in modifying cambium-specific genes Gene editing has been successfully applied to modify cambium-specific genes to understand their roles in secondary growth and wood formation. For instance, the CRISPR-Cas9 system was used to edit the PdBRI1 genes in Populus, which are involved in brassinosteroid signaling. The edited lines exhibited significant changes in cambial activity and wood development, highlighting the importance of these genes in regulating cambium function (Wang et al., 2022a). Similarly, the expression of the co-transcriptional regulator PanNOOT1 in Parasponia andersonii was manipulated using CRISPR-Cas9, demonstrating its essential role in controlling secondary growth (Shen et al., 2021). 6.3 Potential for improving tree stress resistance Gene editing technologies hold great potential for enhancing tree stress resistance by targeting genes involved in stress response pathways. For example, the manipulation of cytokinin signaling pathways through the expression of a constitutively active cytokinin receptor variant in poplar increased cambial activity and stem growth, which could potentially improve the tree's resilience to environmental stresses (Riefler et al., 2022). Additionally, the regulation of brassinosteroid biosynthesis via the overexpression of PagDET2 in poplar promoted cambium cell division and xylem differentiation, suggesting a role in stress adaptation (Wang et al., 2022b).
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 218-228 http://genbreedpublisher.com/index.php/tgmb 225 6.4 Prospects for optimizing breeding strategies The integration of gene editing technologies into tree breeding programs offers promising prospects for optimizing breeding strategies. By precisely modifying genes associated with desirable traits, such as increased biomass production or enhanced stress tolerance, gene editing can accelerate the development of superior tree varieties. For instance, the use of CRISPR-Cas9 to edit genes involved in cambium regulation, such as those in the CLE41/44-PXY-WOX signaling module, can provide insights into the genetic basis of wood formation and facilitate the breeding of trees with improved growth characteristics (Galibina et al., 2023). Furthermore, the ability to manipulate hormonal pathways, such as brassinosteroid and cytokinin signaling, through gene editing can lead to the development of trees with optimized growth and development (Wang et al., 2022a; Riefler et al., 2022). Gene editing technologies offer powerful tools for studying and manipulating cambium-specific genes, improving tree stress resistance, and optimizing breeding strategies. The continued advancement and application of these technologies hold great promise for enhancing researchers’ understanding of cambium regulation and improving the productivity and resilience of forest trees. 7 Concluding Remarks The review of the molecular mechanisms underlying cambium formation and activity maintenance has revealed several critical insights into the collaborative regulation of tree stem cells in growth, development, and environmental adaptation. The identification of receptor-like kinases, such as REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), as opposing regulators of cambium activity, highlights the complexity of signaling pathways involved in secondary growth. Temperature significantly influences cambial reactivation and xylem differentiation, with elevated temperatures leading to earlier cambial reactivation but increasing the risk of frost damage. Hormones such as auxin, cytokinin, gibberellin, and brassinosteroids play cooperative roles in promoting cambium activity, with hormonal pathways acting redundantly to sustain cambium proliferation. Transcription factors, including WOX4 and HD-ZIP III, are crucial in regulating cambium activity and wood formation, with their expression being modulated by environmental and developmental cues. Seasonal changes in cambium activity are accompanied by significant transcriptomic and epigenomic remodeling, affecting gene expression and methylation patterns. The PXY-CLE signaling pathway has been shown to regulate cambial cell division and wood formation, with precise manipulation of this pathway resulting in increased tree growth and productivity. Future research should focus more on the following aspects. Further investigation into the molecular mechanisms of receptor-like kinases and their interaction with other signaling pathways will enhance researchers’ understanding of cambium regulation. Research on the impact of climate change on cambium activity and wood formation will be crucial for developing strategies to mitigate environmental stress in trees. Detailed studies on the interplay between different hormonal pathways and their collective impact on cambium activity will provide insights into optimizing tree growth. Exploring the role of epigenetic modifications in cambium activity and wood formation will help in understanding the long-term adaptation of trees to environmental changes. The identification of key regulatory genes and pathways opens up possibilities for genetic engineering to enhance wood production and stress resilience in trees. The insights summarized in this study have important implications for forestry and tree breeding. By manipulating key regulatory pathways, such as the PXY-CLE signaling pathway, it is possible to increase wood yield and improve tree growth, which is beneficial for timber production and carbon sequestration. Understanding the environmental regulation of cambium activity can aid in breeding trees that are more resilient to climate change, thereby ensuring sustainable forestry practices. The application of genetic engineering techniques to modify the expression of critical genes involved in cambium activity and wood formation can lead to the development of superior tree varieties with desired traits. Insights into the molecular mechanisms of cambium regulation can inform sustainable forestry management practices, optimizing tree growth and wood quality while maintaining ecological balance. By integrating these findings into practical applications, the forestry industry can achieve significant advancements in tree breeding, wood production, and environmental sustainability.
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Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 229-238 http://genbreedpublisher.com/index.php/tgmb 229 Research Insight Open Access The Role of Canopy Management in Optimizing Grapevine Yield and Quality Kaiwen Liang Hainan Institute of Tropical Agricultural Resources, Sanya, 572025, Hainan, China Corresponding email: kaiwen.liang@hitar.org Tree Genetics and Molecular Breeding, 2024, Vol.14, No.5 doi: 10.5376/tgmb.2024.14.0022 Received: 15 Aug., 2024 Accepted: 17 Sep., 2024 Published: 25 Sep., 2024 Copyright © 2024 Liang, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Liang K.W., 2024, The role of canopy management in optimizing grapevine yield and quality, Tree Genetics and Molecular Breeding, 14(5): 229-238 (doi: 10.5376/tgmb.2024.14.0022) Abstract This study explores the critical role of canopy management in optimizing grape yield and quality, emphasizing the principles and practices of enhancing grapevine canopy microclimate to improve production efficiency. Canopy management techniques, including shoot thinning, leaf removal, and pruning systems, contribute to improving light conditions and air circulation within the canopy, thereby optimizing photosynthesis and reducing disease risk. Additionally, the study analyzes the long-term effects of these techniques, such as enhanced sugar accumulation and increased antioxidant content, and examines the potential of automation and precision viticulture technologies to improve management efficiency. Innovative canopy management strategies are particularly essential for achieving sustainable grape cultivation in the face of climate change challenges. Keywords Canopy management; Grape yield and quality; Photosynthesis optimization; Climate change adaptation; Sustainable viticulture 1 Introduction Grapevine canopy management is a critical aspect of viticulture that involves the strategic manipulation of the grapevine's foliage to optimize both yield and quality. This practice encompasses a variety of techniques, including shoot thinning, leaf removal, and trellis training systems, all aimed at improving the microclimate around the grape clusters. Effective canopy management can significantly influence the light environment, which is crucial for the regulation of shoot growth and fruit development. By controlling factors such as shoot density and leaf area, viticulturists can enhance the balance between vegetative and reproductive growth, ultimately leading to improved grape yield and quality (Dry, 2000; Smart et al., 2017). The optimization of yield and quality is of paramount importance in viticulture, as it directly impacts the economic viability and marketability of grape and wine products. Canopy management plays a vital role in this optimization process by influencing key factors such as grapevine water use, berry composition, and the microclimate within the canopy. For instance, practices like shoot trimming and leaf removal can modify the plant's response to soil water availability, thereby preserving wine quality and reinforcing the unique characteristics of the terroir (Pascual et al., 2015; Silvestroni et al., 2016). Additionally, these practices can enhance the grape’s sensory attributes and chemical composition, which are essential for producing high-quality wines (Collins et al., 2020; Petoumenou and Patris, 2021). This study explores the role of canopy management in optimizing grapevine yield and quality. It aims to provide a comprehensive overview of the fundamental principles and practices of canopy management, highlighting its impact on grapevine physiology and fruit development. The study seeks to offer adaptable and efficient canopy management strategy guidelines for various environmental conditions and grapevine varieties. By examining the latest research findings and field trials, it demonstrates how canopy management can be leveraged to achieve the dual goals of high yield and superior grape quality, thereby supporting sustainable viticultural practices. 2 Principles of Canopy Management Canopy management in viticulture refers to the strategic manipulation of the grapevine's foliage to optimize light exposure, air circulation, and ultimately, the yield and quality of the grapes. Key concepts include the control of shoot number, shoot positioning, and leaf removal, which are essential for managing the microclimate within the
Tree Genetics and Molecular Breeding 2024, Vol.14, No.5, 229-238 http://genbreedpublisher.com/index.php/tgmb 230 canopy. These practices aim to balance the vegetative and reproductive growth of the vine, ensuring that the canopy is neither too dense nor too sparse. An optimal canopy density, often around three leaf layers, is advocated to minimize shading and enhance the microclimate for fruit development (Dry, 2000; Smart et al., 2017). The physiological basis of canopy structure in grapevines is rooted in the plant's need to optimize photosynthesis while minimizing stress factors such as excessive shading and poor air circulation. Canopy architecture, including the arrangement and density of leaves, directly influences the vine's ability to intercept light and regulate temperature and humidity around the fruiting zone. Practices such as shoot thinning and leaf removal are employed to modify the canopy structure, enhancing light penetration and reducing the risk of diseases like bunch rot. These adjustments can lead to improved reproductive performance and berry ripening, as seen in studies on varieties like Semillon and Shiraz (Pascual et al., 2015; Silvestroni et al., 2016; Wang et al., 2019). Light interception is a critical factor in grapevine canopy management, as it directly affects photosynthesis, the process by which plants convert light energy into chemical energy. The amount and quality of light reaching the leaves and fruiting zones determine the vine's photosynthetic efficiency and, consequently, its growth and fruit quality (Wedger et al., 2019). Canopy management techniques such as shoot positioning and leaf removal are designed to optimize light distribution within the canopy, enhancing photosynthetic activity and improving grape yield and quality. For instance, increased light interception through canopy porosity adjustments has been shown to positively impact berry composition and hasten fruit maturity, although excessive exposure can lead to flavonoid degradation (Torres et al., 2020; Petoumenou and Patris, 2021; Mataffo et al., 2023). 3 Techniques in Canopy Management 3.1 Pruning strategies Pruning is a fundamental technique in canopy management that significantly influences grapevine yield and quality. It involves the selective removal of certain parts of the vine, such as shoots, leaves, or clusters, to optimize the vine's growth and fruit production. Winter pruning is a common practice that helps control vine vigor and balance the ratio of fruit to foliage, which is crucial for maintaining grape quality (Collins et al., 2020). Pruning strategies can also include shoot thinning, which reduces canopy density and improves light penetration, thereby enhancing the microclimate around the fruiting zone (Dry, 2000). These practices are essential for managing the vine's energy distribution, ensuring that resources are allocated efficiently to produce high-quality grapes. 3.2 Training systems Training systems are designed to shape the grapevine canopy to optimize sunlight exposure and air circulation, which are critical for grape development and disease prevention. Different training systems, such as the Ruakura Twin Two Tier and the Te Kauwhata Three Tier, have been shown to influence canopy architecture and microclimate, thereby affecting yield and fruit composition (Smart et al., 2017). These systems help manage the spatial arrangement of shoots and leaves, reducing shading and promoting uniform ripening of grapes. By adjusting the geometry of the vineyard, training systems can also mitigate the effects of environmental factors, such as temperature and humidity, on grape quality (Pascual et al., 2015). 3.3 Leaf removal practices Leaf removal is a canopy management practice that involves the strategic removal of leaves to improve light exposure and air flow within the canopy. This technique is particularly effective in reducing the incidence of diseases like Botrytis cinerea by decreasing humidity around the fruit clusters (Wang et al., 2019; Mataffo et al., 2023). Leaf removal can be performed at different stages of grape development, such as pre-flowering or pre-veraison, to influence berry composition and ripening (Figure 1) (Gambetta et al., 2020). The removal of leaves can also affect the photosynthetic capacity of the vine, which in turn impacts the sugar accumulation and overall quality of the grapes. By carefully managing leaf area, growers can enhance the microclimate of the canopy, leading to improved grape quality and yield.
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