Hiroyuki Koyama
Chao-Feng Huang
Miguel A. Piñeros
Yoko Yamamoto- 1Applied Biological Sciences, Gifu University, Gifu, Japan
- 2Shanghai Center for Plant Stress Biology, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS), Shanghai, China
- 3Robert W. Holley Center for Agriculture & Health, USDA Agricultural Research Service (USDA-ARS), Ithaca, NY, United States
- 4Institute of Plant Science and Resources, Okayama University, Kurashiki, Japan
Editorial on the Research Topic
Al-Induced and -Activated Signals in Aluminium Resistance
As phytotoxic aluminum (Al) appears in the acid soil at pH <5.5 (Kobayashi et al., 2013), plants have evolved resistance mechanisms to cope with the Al rhizotoxicity (Daspute et al., 2017). Research in this field has identified various constitutive and induceble Al resistance mechanisms that protect Al-sensitive cells in the roots (Daspute et al., 2017). For example, exudation of organic acid (OA) from the roots protects the sensitive cells by chelating the phytotoxic Al3+ to less toxic Al-OA chelated compounds. This OA exudation is controlled by both Al-activated and Al-inducible mechanisms, as reported for the malate transporter ALMT1 (ALUMINUM ACTIVATED MALATE TRANSPORTER 1) in various plant species (Wu et al., 2018). In addition, recent studies identified pleiotropic roles of Al tolerant proteins such as SENSITIVE TO PROTON RHIZOTIXICITY1 (STOP1) (Koyama et al., 2021; Sadhukhan et al., 2021b) and ALMT1 (Wu et al., 2018). The level of such proteins play crucial role to manage Al tolerance and growth response (Fang et al., 2021a). This Research Topic, “Al-Induced and -Activated Signals in Aluminium Resistance,” aimed to enrich our knowledge, enabling a better understanding of the complexity underlining Al resistance mechanisms. The Research Topic contains six original research articles, including three studies using the model species Arabidopsis and three others in crops species, namely tomato, lentil, and cicer.
The studies in Arabidopsis focused on the transcription factor STOP1-regulated system. This extensively studied zinc finger transcription factor regulates the expression of several genes, such as AtALMT1, critical for Al resistance (Sadhukhan et al., 2021b). AtALMT1-expression requires direct binding of STOP1 to the promoter, while the activity and amounts of STOP1 are regulated by complex mechanisms, including posttranslational modification. Huang's group reported several signaling proteins involved in the process of controlling STOP1 using rae (REGULATION OF ATALMT1 EXPRESSION) mutants with altered AtALMT1 expression levels. For example, RAE1, an F-box protein component of a SCF-type E3 ligase complex, alters AtALMT1 expression by degradation of STOP1 through ubiquitination (Zhang et al., 2019), while the SUMO protease RAE5/EARLY IN SHORT DAYS 4 (ESD4) and SUMO E3 ligase SIZ1 can influence AtALMT1 expression by deSMOylation and SUMOylation of STOP1, respectively (Fang et al., 2021b; Xu et al., 2021). In addition, RAE3, a core component of the THO/TREX complex, regulates AtALMT1 expression by modulating nucleocytoplasmic STOP1 mRNA export and consequently influencing the STOP1 protein accumulation. In the current Topic, Zhu et al. provided additional information on RAE2/TEX1, another core component of the THO complex, which is also involved in the regulation of Al resistance and low Pi response by regulating AtALMT1 expression level. Interestingly, rae2 did not show defective nucleocytoplasmic STOP1 mRNA export but accumulated less STOP1 protein and consequently had reduced expression of AtALMT1. It appears that THO-complex, possibly conjugated with mRNA, plays essential role in regulating STOP1's downstream Al resistant genes and development.
On the other hand, Agrahari et al. implemented a Genome-Wide Association (GWAS) to explore the upstream region of STOP1-regulated Al resistant genes. POLYGARACTRONASE INHIBITOR PROTEIN 1 (PGIP1), a stabilizing cell wall pectin, possesses STOP1 binding cis-elements in its promoter and showed Al-inducible expression. eGWAS identified a STOP1-independent NO signaling pathway and a STOP1-dependent regulation in the phosphatidylinositol (PI) signaling pathway, involved in the regulation of PGIP1 expression under Al stress. The former included one of the TRX superfamily proteins, while the latter included NAC027 and an R-R-type MYB transcription factors. A similar eGWAS approach provided further genetic evidence that PI signaling is also involved in the regulation of the Al-resistance gene ALUMINUM SENSITIVE3 (ALS3), possibly through the activation of STOP1 (Sadhukhan et al., 2021a). Furthermore, that study identified the involvement of a Ca signaling pathway in the Al inducible ALS3 expression, which would be independent of the STOP1 pathway.
Desnos and coworkers previously studied the activation of STOP1 in response to P-deficiency in gel medium, providing evidence that the STOP1-activation could occur in the absence of Al stress (Balzergue et al., 2017). In the current topics, the authors (Le Poder et al.) discovered that the STOP1-AtALMT1 pathway could be activated by Al at a level that does not inhibit root growth of the Al-hypersensitive mutant stop1, suggesting that Al signaling can be uncoupled from its toxicity. Furthermore, they found that Al and iron (Fe) can play a synergistic role in activating the STOP1-AtALMT1 pathway. These three studies in Arabidopsis provided new insight into the STOP1-dependent Al signaling, including a very sensitive response to Al, a coordinated regulation with other signaling pathways (i.e., PI, NO, and Ca signaling), and the complex regulation at the STOP1 level via the THO-complex. On the other hand, the regulation of various stress tolerance responses (e.g., Al, proton, P-deficiency hypoxia, and drought) by STOP1 could be referred to as pleiotropy of stress tolerance reported in Arabidopsis and other plants.
Three other manuscripts describe Al signaling and tolerance responses in crop plants. The AAEs (acyl-activating enzymes superfamily) are involved in multiple metabolic pathways, with some of them identified as being related to Al tolerance, Jin et al. studied the expression of AAEs in tomato under aluminum stress. A synteny analysis of AAEs in tomato and Arabidopsis and cis-element predictions suggested that some Al-inducible AAEs carry STOP1-binding motifs in the promoter. Lentil is one of India's oldest cultivating legume and is currently grown as a winter legume. Singh et al. studied inter-and intraspecies transcriptomes that identify different metabolic pathways regulating Al tolerance in lentil. The main upregulated and differentially expressed genes (DEGs) identified under stress conditions are underline organic acid synthesis and exudation, production of antioxidants, callose synthesis, protein degradation, and phytohormone- and calcium-mediated signaling pathways. These genes and pathways are homologous to those Al-inducible processes described in model plants. The study also identified several transcription factors upregulated in tolerant varieties and wild species, probably associated with auxin signal. These findings represent a novel and useful target to improve lentils' Al tolerance using expression-level polymorphisms. Finally, Vance et al. reported Al resistance in wild cicer, a relative species of chickpea. The authors conducted a large-scale screening of Al and low pH tolerance using relative root elongation as a tolerance index, resulting in the identification of resistant cultivars associated with the original locations. Although this study did not focus on Al signaling, it provides novel information on Al resistant varieties of chickpea, a commercially important legume.
This Research Topic shine shed some light in compiling crucial information for a better understanding of the complex signaling involved in the response to Al stress. We welcome readers to explore the six research papers for deeper analysis of their findings.
Author Contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.
Funding
HK was funded by JSPS (KAKENHI and 21H02088).
Conflict of Interest
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.
Publisher's Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Acknowledgments
We thank all authors who contributed to this Research Topic, and those who kindly reviewed the manuscript. We also thank the support of the professional editorial staff at Frontiers.
References
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Daspute, A. A., Sadhukhan, A., Tokizawa, M., Kobayashi, Y., Panda, S. K, and Koyama, H. (2017). Transcriptional regulation of aluminum-tolerance genes in higher plants: clarifying the underlying molecular mechanisms. Front. Plant Sci. 8, 1358. doi: 10.3389/fpls.2017.01358
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Fang, Q., Zhou, F., Zhang, Y., Singh, S., and Huang, C.-F. (2021a). Degradation of STOP1 mediated by the F-box proteins RAH1 and RAE1 balances aluminum resistance and plant growth in Arabidopsis thaliana. Plant J. 106, 493–506. doi: 10.1111/tpj.15181
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Sadhukhan, A., Agrahari, R. J., Wu, L., Watanabe, T., Nakano, Y., Panda, S. K., et al. (2021a). Expression genome-wide association study identifies that phosphatidylinositol-derived signalling regulates ALUMINIUM SENSITIVE3 expression under aluminium stress in the shoots of Arabidopsis thaliana. Plant Sci. 302, 110711. doi: 10.1016/j.plantsci.2020.110711
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Wu, L., Kobayashi, Y., Wasaki, J., and Koyam, H. (2018). Organic acid excretion from roots: a plant mechanism for enhancing phosphorus acquisition, enhancing aluminum tolerance, and recruiting beneficial rhizobacteria. Soil Sci. Plant Nutr. 64, 697–704. doi: 10.1080/00380768.2018.1537093
Xu, J., Zhu, J., Liu, J., Wang, J., Ding, Z., and Tian, H. (2021). SIZ1 negatively regulates aluminum resistance by mediating the STOP1-ALMT1 pathway in Arabidopsis. J. Integr. Plant Biol. 63, 1147–1160. doi: 10.1111/jipb.13091
Keywords: aluminum, signaling, STOP1, Arabidopsis, legume
Citation: Koyama H, Huang C-F, Piñeros MA and Yamamoto Y (2022) Editorial: Al-Induced and -Activated Signals in Aluminium Resistance. Front. Plant Sci. 13:925541. doi: 10.3389/fpls.2022.925541
Received: 21 April 2022; Accepted: 20 May 2022;
Published: 22 June 2022.
Edited by:
Douglas S. Domingues, São Paulo State University, Campus Rio Claro, BrazilReviewed by:
Jorge Fernando Pereira, Embrapa Gado de Leite, BrazilCopyright © 2022 Koyama, Huang, Piñeros and Yamamoto. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Hiroyuki Koyama, koyama@gifu-u.ac.jp