Molecular Plant Breeding 2024, Vol.15 http://genbreedpublisher.com/index.php/mpb © 2024 GenBreed Publisher, registered at the publishing platform that is operated by Sophia Publishing Group, founded in British Columbia of Canada. All Rights Reserved. Publisher
Molecular Plant Breeding 2024, Vol.15 http://genbreedpublisher.com/index.php/mpb © 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 molecular genetics, plant genes or traits, and plant breeding 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 Molecular Plant Breeding Email: edit@mpb.genbreedpublisher.com Website: http://genbreedpublisher.com/index.php/mpb Address: 11388 Stevenston Hwy, PO Box 96016, Richmond, V7A 5J5, British Columbia Canada Molecular Plant Breeding (ISSN 1923-8266) is an international, 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 areas of transgene, molecular genetics, crop QTL analysis, germplasm genetic diversity, and advanced breeding technologies. Molecular Plant Breeding is archived in LAC (Library and Archives Canada) and deposited in CrossRef. The Journal has been indexed by ProQuest as well. The Journal is expected to be indexed by PubMed and other databases in near future. All the articles published in Molecular Plant 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.
Molecular Plant Breeding (online), 2024, Vol. 15 ISSN 1923-8266 http://genbreedpublisher.com/index.php/mpb © 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 Research Progress of NAC Transcription Factor Family in Plant Stress Resistance Ziyi Zhu, Xia An, Xiahong Luo, Changli Chen, Tingting Liu, Lina Zou, Guanlin Zhu Molecular Plant Breeding, 2024, Vol. 15, No. 3, pp.90-99 Expanding Genetic Horizons: The Role of MAGIC Populations in Enhancing Plant Breeding Efficiency Liangrong Jiang, Wanying Xu Molecular Plant Breeding, 2024, Vol. 15, No. 3, pp.100-111 From Ancestors to Modern Cultivars: Tracing the Origin, Evolution, and Genetic Progress in Cucurbitaceae Xuehao Chen, Xiaohua Qi, Xuewen Xu Molecular Plant Breeding, 2024, Vol. 15, No. 3, pp.112-131 Gene-Driven Future: Breakthroughs and Applications of Marker-Assisted Selection in Tree Breeding Yufen Wang, Lianming Zhang Molecular Plant Breeding, 2024, Vol. 15, No. 3, pp.132-143 Precise Editing and Functional Verification of Pine Disease Resistance Genes Yali Deng, Meifang Li Molecular Plant Breeding, 2024, Vol. 15, No. 3, pp.144-154
Molecular Plant Breeding 2024, Vol.15, No.3, 90-99 http://genbreedpublisher.com/index.php/mpb 90 Review and Progress Open Access Research Progress of NAC Transcription Factor Family in Plant Stress Resistance Ziyi Zhu1,2, XiaAn1 , Xiahong Luo1, Changli Chen1, Tingting Liu1, LinaZou1, Guanlin Zhu1 1 Zhejiang Institute of Landscape Plants and Flowers (Zhejiang Xiaoshan Cotton and Hemp Research Institute), Zhejiang Academy of Agricultural Sciences, Hangzhou, 311251, Zhejiang, China 2 College of Environment and Resources, College of Carbon Neutrality, Zhejiang A&F University, Hangzhou, 311300, Zhejiang, China Corresponding email: anxia@zaas.ac.cn Molecular Plant Breeding, 2024, Vol.15, No.3 doi: 10.5376/mpb.2024.15.0011 Received: 27 May., 2024 Accepted: 20 Jun., 2024 Published: 25 Jun., 2024 Copyright © 2024 Zhu 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: Zhu Z.Y., An X., Luo X.H., Chen C.L., Liu T.T., Zou L.N., and Zhu G.L., 2024, Research progress of NAC transcription factor family in plant stress resistance, Molecular Plant Breeding, 15(3): 90-99 (doi: 10.5376/mpb.2024.15.0011) Abstract NAC (NAM, ATAF1/2, and CUC2) transcription factors are a class of plant specific transcription factor genes with numerous family members, commonly found in higher plants, and also found in moss plants. The N-terminus of these genes has a highly conserved NAC domain. It plays a crucial role in the growth and development of plants, as well as in their response to biotic stress (such as insects and plant pathogens) and abiotic stress (such as drought, salinity, temperature, and heavy metals). This article introduces the basic characteristics of the NAC transcription factor family and briefly elaborates on its research in plant stress resistance in recent years, providing some reference for future research on the stress resistance of NAC transcription factors. Keywords Transcription factors; NACgene; Resistance to adversity; Plant 1 Introduction Plants, as primary producers in ecosystems, have been exposed to a number of unfavorable environments during their long evolution, mainly including biotic stresses and abiotic stresses. Studies have shown that annual yield losses due to biotic stresses are estimated to be about 35% and abiotic stresses can lead to more than 50% yield losses (Mukhtar and Stockle, 2016). In order to survive and reproduce, plants have evolved complex mechanisms to sense environmental changes and respond adaptively, in which transcription factors play an extremely important regulatory role. Transcription factors are a crucial component of gene regulation; they are a set of protein molecules that specifically bind to particular sequences upstream of the 5' end of genes, ensuring the expression of target genes in precise temporal and spatial patterns. In plant systems, such molecules play an indispensable role in regulating plant growth and development as well as adaptive responses to environmental stresses, and NAC, WRKY, MYB, MYC, bZIP, DREB, and CBF are some of the more common transcription factors. Among them, the NAC transcription factor family is one of the important transcription factor families in plants, and the name of this transcription factor family comes from the NAMgene in the Petunia × hybrida hort. ex Vilm, the ATAF1 and ATAF2 genes in Arabidopsis thaliana, and the CUC2 gene. In this paper, the basic structural features of the NAC transcription factor family are described in detail, and the related research progress in plant stress tolerance is sorted out and analyzed in the hope of providing a certain theoretical basis for the study of stress tolerance of the NAC transcription factor family. There are many members of the NAC transcription factor family, and each of the members plays a unique function in the response to a specific biotic or abiotic stress. In recent years, the research on NAC transcription factors has made remarkable progress in plant stress tolerance. The following table summarizes the functions of different NAC transcription factors in response to abiotic (Table 1) and biotic (Table 2) stresses in different plants. 2 Characterization of the NAC Transcription Factor Family The NAC family of transcription factors has a distinctive structural feature (Figure 1), the amino acid-terminal-containing NAC structural domain, consisting of 150~160 amino acid residues, which is responsible
Molecular Plant Breeding 2024, Vol.15, No.3, 90-99 http://genbreedpublisher.com/index.php/mpb 91 for DNA binding and is the basis for the NAC proteins to recognize and bind specific DNA sequences. The domain contains five subdomains (A to E), including conserved subdomains A, C, and D, and diverse subdomains B and E. Based on differences in sequence homology, this family can be systematically classified into two major categories: the first integrates 14 unique subclassifications, counting TERN, ONAC022, SENU5, NAP, AtNAC3, ATAF, OsNAC3, NAC2, ANAC011, TIP, OsNAC8, OsNAC7, NAC1, and NAM. Different subfamilies of NAC proteins showed functional specificity. For instance, the ATAF subfamily, also known as subfamily III-1, has been substantiated through research to have its members extensively involved in various biotic and abiotic stress responses (Ou et al., 2024); the second group, on the other hand, encompasses four subclassifications, namely ANAC001, ONAC003, ONAC001 and ANAC063 (Lu et al., 2024). Table 1 Non biological stress-related NAC transcription factors NACgene Stress resistance function Species Literature ANAC096 Positive regulation of drought tolerance Arabidopsis thaliana (Xu et al., 2013) OsNAC3 Positive regulation of salt and alkaline tolerance Oryza sativa (Zhang et al., 2021a) ZmNAC074 Positive regulation of heat resistance Arabidopsis thaliana (Xi et al., 2022) GmNAC20 Positive regulation of salt and cold tolerance Arabidopsis thaliana (Hao et al., 2011) CaNAC2 Positive regulation of cold tolerance Capsicum annuum (Guo et al., 2015) AmNAC24 Positive regulation of cold tolerance Ammopiptanthus mongolicus (Dorjee et al., 2024) MsNAC001 MsNAC058 Positive regulation of salt alkaline and drought resistance Medicago sativaL. (Min et al., 2020) Table 2 NAC transcription factors related to biological stress NACgene Stress resistance function Species Literature ANAC019 ANAC055 Changing resistance to gray mold Arabidopsis thaliana (Bu et al., 2008) GhNAC100 Changing resistance to Dahlia wilt pathogen Cotton (Hu et al., 2019) TaNAC069 Enhancing resistance to leaf rust fungus Wheat (Zhang et al., 2021b) The carboxyl-terminus (C-terminus), on the other hand, is the transcriptional activation domain (TAD), which is less conserved and has a high degree of diversity, and plays a decisive role in the functional specificity of transcription factors such as activation or repression of gene expression. For example, the five sub-structural domains (A-E) in Arabidopsis, which are differently conserved, contain multiple chemical modification sites and hydrophobic regions. Subdomain D may be related to DNA binding and nuclear localization, while the C-terminal F and G regions may be related to transcriptional activation functions and secondary growth NAC subfamily delineation (Chen et al., 2009). Figure 1 Structural characteristics of NAC transcription factors (Adopted from Puranik et al., 2012)
Molecular Plant Breeding 2024, Vol.15, No.3, 90-99 http://genbreedpublisher.com/index.php/mpb 92 NAC transcription factors are a family of transcription factors unique to plants and not found in animals or microorganisms, and the NAC family is one of the largest families of transcription factors in plants, with the number of members varying greatly among plant species. For example, in Arabidopsis thaliana, about 150 NAC transcription factors are known; in rice, there are more than 300 NAC family members; and in soybean there are 152 each (Sun et al., 2012); and 163 genes in poplar (Han et al., 2023). The variation in the number of NAC transcription factor families in different plants not only reflects the differences in genome size and complexity, but also plays different roles in plant stress response. 3 Role of NAC Transcription Factors in Abiotic Stresses NAC transcription factors play an important role in abiotic stresses, which mainly include environmental stresses, including drought, salinity, low temperature, high temperature, heavy metal pollution, ultraviolet radiation, and nutrient deficiency. 3.1 Drought stress Drought stress is a phenomenon that affects normal plant growth and development due to a severe shortage of water content in the soil or a reduction in plant-available water caused by environmental conditions. Studies have shown that NAC transcription factors play an important role in regulating plant responses to drought stress. For example, when rice is subjected to drought stress during its reproductive period, overexpression of the stress responsive gene SNAC1 (STRESS-RESPONSIVE NAC1) can improve the drought tolerance of transgenic rice and increase the seed setting rate by 22%~34%. During the nutritional growth period, genetically modified rice also showed excellent drought resistance. Compared to wild-type rice, genetically modified rice has significantly increased sensitivity to abscisic acid (ABA), and research has found that, The SNAC1 gene is mainly induced and expressed in guard cells under drought conditions, and its encoded protein is a transcriptional activating NAM ATAF and CUC (NAC) transcription factors effectively slow down water loss and improve plant drought resistance by closing stomatal pores more frequently, but this process did not significantly affect their photosynthesis rate (Hu et al., 2006). And in sweet potatoes, there is a pressure induced IbNAC3, which is a transcription activator located in the nucleus and contains a unique activation domain that can interact with ANAC011 The interaction between ANAC072, ANAC083, ANAC100, and NAP enhances plant tolerance to drought environments in Arabidopsis by overexpressing IbNAC3 (Meng et al., 2022). In addition, SlNAC6 (SlNAC6-RNAi) plays an important role in tomato development, drought stress response, and fruit ripening. Studies have shown that some of its effects may be achieved through the regulation of ABA mediated pathways. Overexpression of SlNAC6 leads to a decrease in water loss rate and degree of oxidative damage in tomatoes, as well as an increase in proline content and antioxidant enzyme activity, thereby improving plant drought resistance (Jian et al., 2021). Research has found that six ZmNAC genes found in maize can significantly enhance plant drought tolerance (Wang et al., 2020a). For example, the ZmNAC48 gene in maize has been shown to enhance drought tolerance in Arabidopsis. However, this gene has a natural antisense transcript cis NATZmNAC48, which has a negative regulatory effect on ZmNAC48. When cis-NATZmNAC48 is overexpressed, it interferes with the normal function of ZmNAC48, thereby affecting the normal closure of maize stomata, leading to a decrease in maize drought resistance (Mao et al., 2021). In addition, overexpression of the apple MdNAC29 gene reduces the drought resistance of apple plants, callus tissues, and tobacco, and exhibits higher relative conductivity, malondialdehyde (MDA) content, and lower chlorophyll content under drought stress (Li et al., 2023). Another study found that under drought conditions, overexpression of LpNAC13 in lily bulbs in tobacco resulted in a decrease in plant antioxidant enzyme activity, proline, and chlorophyll content, The MDA content increased, while the results under salt conditions were opposite to those under drought conditions. Overexpression of LpNAC13 in tobacco reduces its drought resistance and enhances its salt tolerance (Wang et al., 2020b). 3.2 Salt stress Salt stress is one of the major abiotic stresses that constrain plant growth and development, and to cope with these unfavorable factors, plants adopt a series of strategies, such as synthesizing osmoregulatory substances, increasing
Molecular Plant Breeding 2024, Vol.15, No.3, 90-99 http://genbreedpublisher.com/index.php/mpb 93 the activity of antioxidant enzymes, and maintaining ionic homeostasis, in order to mitigate the negative effects of saline stress on their growth and development. Some of the NAC transcription factors depend on the ABA pathway to regulate salt tolerance in plants. For example, rice OsNAC3 is an important regulator of ABA signaling response and salt tolerance. the expression of genes such as Os HKT1;4, Oshkt1;5, Oslea3-1, Ospm-1, Ospp2C68, and Osrab-21 reduced its sensitivity to abscisic acid and improved plant tolerance to salt stress (Zhang et al., 2021a). Overexpression of GmSIN1 in soybean promoted root growth and increased yield under salt stress. Its response to salt stress requires rapid induction of ABA (abscisic acid) and ROS (reactive oxygen species). Further studies revealed that GmSIN1, GmNCED3s and GmRbohBs synergistically formed a positive feed-forward regulatory mechanism, which significantly accelerated the process of ABA and ROS accumulation, thereby amplifying salt stress signals and enabling the plant to respond to and adapt to the salt-stressed environment more rapidly (Li et al., 2019). Some NAC transcription factors do not rely on the ABA pathway and regulate plant salt tolerance. Overexpression of Pennisetum glaucumPgNAC21 in Arabidopsis enhances GSTF6 (glutathione s-transfer 6), The expression of COR47 (cold regulated 47) and RD20 (responsive to dehydration 20) enhances plant salt tolerance (Shinde et al., 2019). Overexpression of Ts NAC1 gene in Thellungiella salsuginea and Arabidopsis can enhance plant tolerance to drought, cold, and salt stress, thereby delaying plant growth rate (Liu et al., 2018a). A high salt environment can also induce the expression of OsNAC071 in rice, thereby improving plant salt tolerance (Liu, 2023). In addition, salt stress and alkali stress are two different abiotic stresses, but they are often collectively referred to as salt stress, and alkali stress tends to cause more significant damage to plants (Wang et al., 2017). However, these two stresses often occur together, and high concentrations of salt and alkaline environments can cause multiple adverse effects on plant root cells. It was found that LpNACl3 and LpNAC5 could enhance the seed germination rate under saline and alkaline stress to a certain extent, and significantly enhance the salt and alkali tolerance of transgenic tobacco seedlings, but would reduce their drought tolerance to a certain extent (Wang, 2020). The transgenic tobacco seedlings were found to be more tolerant to salt and alkali. And this phenomenon was also reflected in LpNAC6, where antioxidant enzymes (SOD, POD, CAT) activities, chlorophyll content, proline content and photosynthetic capacity were increased in LpNAC6 transgenic tobacco, while MDA, H2O2 and O2-contents were reduced, which enhanced alkali tolerance, but showed the opposite effect under drought stress (Yan et al., 2022). 3.3 Temperature stress Temperature stress refers to environmental temperatures that exceed the optimal growth range of plants, and includes two main forms of low-temperature stress and high-temperature stress, which can adversely affect plant growth, development, physiology, and survival. Low-temperature stress is also divided into cold damage (0 ℃~15 ℃) and freezing damage (below 0 ℃), both of which can cause different degrees of damage to plants, but the mechanisms are different, with freezing damage involving the formation of ice crystals directly physically damaging the cells, whereas cold damage leads to damage more through disruption of physiological processes Cold damage is more likely to result in injury through disruption of physiological processes (Lu et al., 2024). Overexpression of LlNAC2 in Arabidopsis thaliana enhances the resistance of Lilium lancifolia to cold stress by participating in the DREB/CBF-COR and ABA signaling pathways in cold stress (Yong et al., 2019). CaNAC064 isolated from pepper leaves has transcriptional activation activity at a critical region of 691~1 071 bp, which can interact with low-temperature-induced monomeric-type proteases to positively regulate cold resistance in plants (Hou et al., 2020). At 0 ℃~15 ℃, overexpression of MdNAC104 enhanced the antioxidant enzyme activities of apple plants and attenuated the damage of PSII, thereby enhancing the cold tolerance of the plants. In addition, below 0 ℃, overexpression of MdNAC104 in apple plants affected the accumulation pattern of osmoregulatory substances in the stem and leaves, and improved cold tolerance (Mei, 2023).
Molecular Plant Breeding 2024, Vol.15, No.3, 90-99 http://genbreedpublisher.com/index.php/mpb 94 High temperature stress occurs when the ambient temperature reaches or exceeds the maximum temperature threshold for plant growth. This stress may lead to problems such as reduced photosynthetic efficiency, altered protein structure, and increased membrane lipid peroxidation in plants, which in turn affects flowering and fruiting and may cause tissue damage, such as standing wilt in seedlings. It has been found that in response to high-temperature stress, plants synthesize heat-stimulated proteins (HSPs), which are usually regulated by heat-stimulated transcription factors (HSFs). NAC019 overexpressed in Arabidopsis thaliana was able to bind to the promoters of HSFA1b, HSFA6b, HSFA7a, and HSFC1, increasing the heat tolerance of plants (Guan et al., 2014). Under high-temperature treatment, by transferring the TaNAC2 gene from wheat to Arabidopsis, the hypocotyl growth length of transgenic TaNAC2L Arabidopsis significantly exceeded that of wild-type plants, and expression levels of six thermally induced genes in Arabidopsis notably surpassed those in the wild type, implying that TaNAC2L enhances thermal resistance by orchestrating the expression of stress-related genes (Guo et al., 2015). When overexpressed in transgenic Arabidopsis, ZmNAC074 isolated from corn significantly enhances plant tolerance to high-temperature environments by regulating various stress metabolites such as reactive oxygen species (ROS), malondialdehyde (MDA), proline, soluble protein, chlorophyll, and carotenoids (Xi et al., 2022). The involvement of NAC transcription factors can appropriately regulate the mechanism of plant response to temperature stress, helping plants to adapt and resist these adverse environmental factors to a certain extent. In addition, ATAF1 in Arabidopsis thaliana is negatively regulated under high-temperature environment. ATAF1 knockout mutants exhibited better heat tolerance compared to the wild type in the experiment (Alshareef et al., 2022). 3.4 Heavy metal stress Heavy metal stress refers to the presence of heavy metal ions in the environment, such as Cd Mn, Pb, Cd, and Hg, etc, present in the environment at too high a concentration, negatively affect organisms (especially plants). When these heavy metal ions enter the plant body, they interfere with normal physiological and biochemical processes and induce a series of defense responses. Research has found that NAC transcription factors fromAegilops markkrafii can reduce cadmium concentration in transgenic wheat. Under excessive cadmium treatment, the transcription of AemNAC2 and AemNAC3 is upregulated approximately 150 times, Overexpression of AemNAC2 in the wheat variety "Bobwhite" leads to a decrease in cadmium concentration in roots, aboveground parts, and grains (Du et al., 2020). In addition, IDEF2 (Iron deficiency responsive cis acting element 2) in the rice NAC family can maintain Fe stability in rice tissues (Walker and Connolly, 2008). Another study found that SiNACs in willows exhibit two significant Pb positive reaction patterns (early and late), both containing 10 SiNACs (Xin et al., 2023). In addition, Overexpression of TdNAC8470 in rice increased grain starch concentration but decreased grain Fe The content of Zn and Mn may be involved in regulating grain protein content, starch synthesis, etc. (Gong et al., 2022). 3.5Others In addition to the aforementioned abiotic stresses, plants may also face mineral nutrient stress, light stress, oxidative stress, and mechanical and physical damage. For example, research has found that after dark treatment, more than 1/4 of NAC expression is increased in Arabidopsis leaves (Lin and Wu, 2004); And under strong light, ANAC078 can induce genes related to flavonoid biosynthesis, increase the accumulation of anthocyanins, and cope with high light stress (Morishita et al., 2009). At 0.1% oxygen, the decrease in ANAC102 expression significantly reduces germination efficiency, but the increase in expression has no effect on germination. Arabidopsis ANAC102 is an important regulatory factor for seed germination under flooded conditions (Christianson et al., 2009). Under low phosphorus stress, soybean transcription factor GsNAC1 can regulate the expression of genes in plant roots, stems, and leaves, enhancing soybean tolerance to low phosphorus soil (Xiong et al., 2024).
Molecular Plant Breeding 2024, Vol.15, No.3, 90-99 http://genbreedpublisher.com/index.php/mpb 95 4 Role of NAC Transcription Factors in Biotic Stresses Biotic stress is the combined effects of various biological factors that are detrimental to the survival and development of an organism. These effects usually originate from the activities of other organisms, including diseases caused by pathogens (e.g., viruses, bacteria, fungi), pest infestation, disturbance by parasitic organisms, and damage by competing species (e.g., weeds), etc. NAC can be involved in different pathogen stresses in different plants (Figure 2). There are fewer reports in the existing literature related to the involvement of the NAC transcription factor family in the biological responses of plants, and there are either positive or negative regulatory roles of NAC transcription factors in biotic stresses. Figure 2 The role of NAC transcription factors in biological stress (Adopted from Lu et al., 2024) During the long evolutionary process of plants, a fine-tuned system of disease resistance defense has been developed. This system is mainly composed of three disease resistance signaling pathways, namely: a salicylic acid (SA)-dependent signaling pathway, a jasmonic acid (JA)-dependent signaling pathway, and an ethylene-dependent signaling pathway (Zhou et al., 2017). Many NAC proteins regulate plant defense responses to enhance plant disease resistance by activating PRgenes, inducing hypersensitive response (HR) and cell death at the site of infection (Nuruzzaman et al., 2013). It was found that ONAC122 and ONAC131 were induced to be expressed under the infestation of Botrytis cinerea. And, ONAC122 and ONAC131 were induced by salicylic acid, methyl jasmonate, or 1-aminocyclopropane-1-carboxylic acid (precursor of ethylene) treatment (Sun et al., 2013). ONAC066 positively regulates rice resistance to rice blast and leaf blight, and ONAC0666 exerts its disease resistance function by regulating the ABA signaling pathway, sugar and amino acid accumulation in rice (Liu et al., 2018b). In addition, by overexpressing the OsNAC60 gene, the transgenic plant exhibit improved resistance to rice blast, whereas when the miR164a/OsNAC60 regulatory module was dysfunctional, rice was significantly susceptible to Rickettsia spp. infection. Further studies found that Osa-miR164a, on the other hand, promotes the infection of B. oryzae (Wang et al., 2018). Except for rice, some NAC genes of other plants also play an important role in disease resistance response. In B. juncea, BjuNAC62 Δ C can enhance resistance to the black spot pathogen of Chinese cabbage (Mondal et al., 2022). The TaNAC069 gene plays a positive regulatory role in the resistance of wheat to leaf rust (Zhang et al., 2021b). The barley leaf rust resistance gene locus Rph7 has been shown to exhibit abnormally high sequence and haplotype differences, and it shares structural similarities with the N-terminal DNA binding domain of the NAC transcription factor (ANAC019) from Arabidopsis, Rph7 is presumed to be a NAC transcription factor (Chen et al., 2023).
Molecular Plant Breeding 2024, Vol.15, No.3, 90-99 http://genbreedpublisher.com/index.php/mpb 96 5Prospect Although NAC transcription factors have made significant achievements in the field of plant stress resistance research, there are still many unknown areas waiting to be explored. In order to gain a more comprehensive understanding of the molecular regulatory mechanisms of NAC in plants and provide strong support for growth regulation and stress resistance enhancement, future research can be carried out in the following directions: Firstly, given the numerous and diverse functions of the NAC family, in-depth research on the interactions and synergistic regulatory mechanisms among different members will help us to have a more comprehensive understanding of the role of NAC in plant growth, development, and stress response; Secondly, current research on the role of NAC in stress response mainly focuses on the nutritional growth stage of plants, with limited understanding of its regulatory role in the reproductive stage, which will be an important direction for future research; Finally, by exploring the excellent allele variations of NAC in natural and mutant populations, and exploring their potential applications in improving crop quality, yield, and stress resistance, new strategies and ideas will be provided for genetic improvement of crops. 6 Conclusion NAC transcription factors play a crucial role in the response mechanisms of plants to biotic and abiotic stresses. They can sense various environmental pressure signals, such as drought, salinity, low temperature, etc., thereby activating or inhibiting the expression of a series of downstream genes, helping plants adapt to adverse environmental conditions. This enables us to accurately cultivate new plants with stronger resistance to disease and stress through transgenic technology. Authors’ Contributions ZZ, XA, LZ, GZ, and CC originated the conceptual framework; XA supervised the data compilation; ZZ performed the formal analyses; XA secured the financial support. The research was carried out by ZZ and TL, with methodological guidance from ZZ and XL. Resource acquisition was handled by XA and ZZ. The initial draft of the manuscript was prepared by XA and ZZ, and XA led the subsequent drafting, review, and editing process. All authors read and approved the final manuscript. Acknowledgments This study is funded by the Ministry of Finance and the Ministry of Agriculture and Rural Affairs: the National Bast Modern Agricultural Industry Technology System (CARS-16-S05). Conflict of Interest Disclosure The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest. References Alshareef N.O., Otterbach S.L., Allu A.D., Woo Y.H., de Werk T., Kamranfar I., Mueller-Roeber B., Tester M., Balazadeh S., and Schmöckel S.M., 2022, NAC transcription factors ATAF1 and ANAC055 affect the heat stress response in Arabidopsis, Sci. Rep., 12(1): 11264. https://doi.org/10.1038/s41598-022-14429-x PMid:35787631 PMCid:PMC9253118 Bu Q., Jiang H., Li C.B., Zhai Q., Zhang J., Wu X., Sun J., Xie Q., and Li C., 2008, Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses, Cell Research, 18(7): 756-767. https://doi.org/10.1038/cr.2008.53 Chen C., Jost M., Outram M.A., Friendship D., Chen J., Wang A., Periyannan S., Bartoš J., Holušová K., Doležel J., Zhang P., Bhatt D., Singh D., Lagudah E., Park R.F., and Dracatos P.M., 2023, A pathogen-induced putative NAC transcription factor mediates leaf rust resistance in barley, Nature Communications, 14(1): 5468. https://doi.org/10.1038/s41467-023-41021-2 PMid:37673864 PMCid:PMC10482968 Chen Y., Sun X., Hu S., Cao Y., and Lu X.Q., 2009, Analysis of conserved domains of NAC transcription factors related to secondary growth in Arabidopsis thaliana, Journal of Northwest A&F University (Natural Science Edition), 37(5): 185-194, 200.
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Molecular Plant Breeding 2024, Vol.15, No.3, 100-111 http://genbreedpublisher.com/index.php/mpb 100 Invited Review Open Access Expanding Genetic Horizons: The Role of MAGIC Populations in Enhancing Plant Breeding Efficiency Liangrong Jiang , Wanying Xu Xiamen Plant Genetics Key Laboratory, School of Life Sciences, Xiamen University, Xiamen, 361102, Fujian, China Corresponding email: lrjiang108@xmu.edu.cn Molecular Plant Breeding, 2024, Vol.15, No.3 doi: 10.5376/mpb.2024.15.0012 Received: 07 Jan., 2024 Accepted: 15 Apr., 2024 Published: 26 Jun., 2024 Copyright © 2024 Jiang and Xu, 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: Jiang L.R., and Xu W.Y., 2024, Expanding genetic horizons: the role of MAGIC populations in enhancing plant breeding efficiency, Molecular Plant Breeding, 15(3): 100-111 (doi: 10.5376/mpb.2024.15.0012) Abstract The burgeoning global population and the concomitant demand for increased agricultural productivity necessitate the exploration of innovative breeding strategies. Multi-parent advanced generation inter-cross (MAGIC) populations have emerged as a pivotal resource in plant breeding, offering a unique amalgamation of genetic diversity and recombination. These populations are derived from multiple founder parents and result in recombinant inbred lines (RILs) that serve as a genetic mosaic, capturing a broad spectrum of genetic variation. The development of MAGIC populations, through either "funnel" or "diallel" cross-designs, ensures a balanced representation of each parent's genome, thereby maximizing the potential for genetic discovery and trait improvement. The application of MAGIC populations has been demonstrated across various crops, including cereals, cowpea, sorghum, tomato, eggplant, rice, and strawberry, highlighting their versatility and potential for enhancing breeding efficiency. Advances in genotyping technologies and specific software development have facilitated the genetic analysis of these complex populations, enabling the identification of quantitative trait loci (QTLs) and the selection of elite breeding material. Furthermore, MAGIC populations are instrumental in dissecting complex traits, such as disease resistance, abiotic stress tolerance, and grain quality, and hold promise for the direct release of new varieties. The integration of MAGIC populations into breeding pipelines, coupled with the potential for inter-specific crosses and the development of populations in non-pure line crops, underscores their transformative role in plant breeding. This review underscores the significance of MAGIC populations in advancing genetic research and breeding, paving the way for the development of improved cultivars to meet future agricultural challenges. Keywords MAGIC populations; Plant breeding; Genetic diversity; Recombinant inbred lines; Quantitative trait loci; Crop improvement; Genotyping; Genetic analysis; Trait dissection; Cultivar development 1 Introduction Plant breeding is a critical component of agricultural development, aimed at improving crop yields, resistance to diseases, and adaptation to environmental stresses. However, the complexity of plant genomes and the multifaceted nature of agronomic traits pose significant challenges to breeders. Traditional breeding methods often rely on bi-parental crosses, which can limit the genetic diversity and slow down the breeding process. To overcome these limitations, advanced genetic tools are needed to explore the vast genetic potential within crop species and accelerate the development of improved varieties. One such advanced tool is the Multi-parent Advanced Generation Inter-Cross (MAGIC) population. MAGIC populations are derived from the intercrossing of multiple founder parents, resulting in a diverse and recombined genetic resource. These populations are characterized by their ability to capture a wide array of genetic variation from several different lines, thus providing a powerful platform for genetic analysis and selection of elite breeding material (Cavanagh et al., 2008; Bandillo et al., 2013; Pascual et al., 2015; Wei and Xu, 2015; Meng et al., 2016; Ongom and Ejeta, 2017; Huynh et al., 2018; Campanelli et al., 2019; Arrones et al., 2020; Mangino et al., 2021). The emergence of MAGIC populations represents a significant step forward in plant breeding, as they combine the genetic contributions of multiple parents and facilitate the mapping of QTLs with greater precision. The objectives of this review are to provide an overview of the challenges faced in plant breeding and the need for advanced genetic tools like MAGIC populations, to define and discuss the emergence of MAGIC populations and their design, and to explore how these populations can enhance the efficiency of plant breeding programs. By examining the development and application of MAGIC populations across various crop species, this review aims to highlight their potential in unlocking genetic diversity and driving the next wave of crop improvement.
Molecular Plant Breeding 2024, Vol.15, No.3, 100-111 http://genbreedpublisher.com/index.php/mpb 101 2 Development of MAGIC Populations 2.1 Historical development of MAGIC populations in plant breeding The concept of MAGIC populations represents a significant evolution in plant breeding methodologies. Historically, plant breeding has relied on bi-parental crosses to combine desirable traits. However, the advent of MAGIC populations has expanded the genetic horizons by incorporating alleles from multiple founder parents into a single population. This approach has been increasingly adopted across various crops, including cereals, legumes, and vegetables, to enhance genetic diversity and improve complex traits (Cavanagh et al., 2008; Bandillo et al., 2013; Meng et al., 2016; Ongom and Ejeta, 2017; Huynh et al., 2018; Campanelli et al., 2019; Arrones et al., 2020; Mangino et al., 2021; Samineni et al., 2021; Singh and Shrivastav, 2023). 2.2 Genetic principles and breeding strategies involved in creating MAGIC populations MAGIC populations are constructed by intercrossing a number of diverse founder lines, followed by several generations of mating, which can include both structured and random matings. The resulting RILs are a genetic mosaic of the founder genomes, providing a rich resource for genetic analysis and breeding. The development of these populations can follow "funnel" or "diallel" cross-designs, ensuring a balanced representation of each parent's genome (Huynh et al., 2018; Arrones et al., 2020). The use of advanced genotyping technologies, such as genotyping-by-sequencing (GBS), has facilitated the characterization of these complex populations (Bandillo et al., 2013; Ongom and Ejeta, 2017). The genetic makeup of MAGIC populations allows for the fine mapping of QTLs and the identification of novel alleles for trait improvement (Cavanagh et al., 2008; Samineni et al., 2021). 2.3 Comparison with traditional and other contemporary breeding methodologies Compared to traditional bi-parental crosses, MAGIC populations offer a higher level of recombination and allelic diversity, which is advantageous for dissecting complex traits (Bandillo et al., 2013; Arrones et al., 2020). Unlike other contemporary breeding methods, such as genome-wide association studies (GWAS) that rely on natural populations, MAGIC populations are specifically designed with breeding goals in mind, combining desirable traits from elite breeding lines (Cavanagh et al., 2008). This targeted approach, along with the lack of genetic structure and high phenotypic diversity, makes MAGIC populations a more powerful tool for both gene discovery and the direct enhancement of breeding populations (Meng et al., 2016; Huynh et al., 2018; Campanelli et al., 2019; Mangino et al., 2021; Singh and Shrivastav, 2023). The development of MAGIC populations, despite being resource-intensive, has led to the identification of strong associations and candidate genes for important agronomic traits, thereby contributing to the development of advanced varieties (Mangino et al., 2021; Samineni et al., 2021; Singh and Shrivastav, 2023). In conclusion, the development of MAGIC populations marks a significant milestone in the history of plant breeding, offering a sophisticated tool for expanding genetic diversity and improving crop traits. The strategic intercrossing of multiple parents and the application of advanced genetic analysis have positioned MAGIC populations as a cornerstone for future breeding efforts aimed at meeting global agricultural demands. 3 Advantages of Using MAGIC Populations 3.1 Enhanced genetic diversity and its impact on breeding MAGIC populations are a revolutionary step in plant breeding, offering a genetic mosaic derived from multiple founder parents. This results in high genetic and phenotypic diversity, which is essential for the exploitation of plant genetic resources (Arrones et al., 2020). The development of MAGIC populations in crops like cowpea has incorporated a wide array of traits from genetically diverse founders, including resistance to abiotic and biotic stresses, seed quality, and agronomic traits (Huynh et al., 2018). This diversity is a cornerstone for breeding programs aiming to improve crop varieties by combining desirable traits from different lines. 3.2 Improved resolution of QTLs mapping MAGIC populations have proven to be powerful tools for the dissection of complex traits. The sorghum MAGIC population, for example, has shown that a significant proportion of founder alleles segregate within the population, allowing for high-resolution mapping of QTLs (Ongom and Ejeta, 2017). Similarly, in eggplant, the development of a MAGIC population has enabled the identification of strong associations and candidate genes for anthocyanin
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