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Plant Commun
Plant Commun
Plant Communications
2590-3462
Elsevier

S2590-3462(24)00324-9
10.1016/j.xplc.2024.101007
101007
Commentary
Leveraging a new thermosensor for heat-smart future agriculture
Raza Ali 1234
Zaman Qamar U. 56
Hu Zhangli huzl@szu.edu.cn
134∗
1 Guangdong Key Laboratory of Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China
2 College of Physics and Optoelectronic Engineering, Shenzhen University, Shenzhen 518060, China
3 Shenzhen Engineering Laboratory for Marine Algal Biotechnology, Guangdong Technology Research Center for Marine Algal Biotechnology, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China
4 Shenzhen Collaborative Innovation Public Service Platform for Marine Algae Industry, Longhua Innovation Institute for Biotechnology, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China
5 School of Breeding and Multiplication (Sanya Institute of Breeding and Multiplication), Hainan Yazhou-Bay Seed Laboratory, Hainan University, Sanya 572025, China
6 Collaborative Innovation Center of Nanfan and High-Efficiency Tropical Agriculture, School of Tropical Crops, Hainan University, Haikou 570228, China
∗ Corresponding author huzl@szu.edu.cn
22 6 2024
09 9 2024
22 6 2024
5 9 1010076 6 2024
19 6 2024
21 6 2024
© 2024.
2024

https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Published: June 22, 2024
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pmcMain text

As global temperatures rise owing to climate change, crops are increasingly subjected to conditions that surpass their optimal temperature ranges, leading to heat stress (HS). HS impacts many morpho-physiological, biochemical, and molecular mechanisms in plants, ultimately affecting sustainable agricultural production worldwide (Ding et al., 2020; Kan et al., 2023; Raza et al., 2024). The increased frequency and intensity of HS also threaten crop hardiness, necessitating the design of heat-smart cultivars to sustain agricultural productivity (Ding et al., 2020; Kan et al., 2023; Raza et al., 2024). To mitigate these impacts, we need to acquire more insights into the molecular pathways that underlie HS responses in plants and discover new regulators that can be targeted for breeding or biotechnological interventions.

Despite noteworthy innovations in understanding HS responses and tolerance mechanisms, how plants perceive HS signals remains an open question. To address this, Bohn et al. (2024) recently discovered a new thermosensor in Arabidopsis, THERMO-WITH ABA-RESPONSE 1 (TWA1), that marks a significant breakthrough and offers new hope for heat-smart agriculture (Figure 1). It functions as a gene-regulatory protein that helps plants manage HS by altering the expression of stress-responsive genes. TWA1 was recognized through its role in regulating ABA-responsive genes, which are essential for plant responses to diverse stresses. The TWA1 protein acts as a transcriptional co-regulator, interacting with JASMONATE-ASSOCIATED MYC-LIKE (JAM) transcription factors (TFs) and TOPLESS (TPL) co-repressors. These interactions are essential for development of the repressor complexes that transform gene expression under temperature shifts (Figures 1B–1D). One of the key discoveries is that TWA1-mediated inhibition of ABA-responsive gene expression is temperature dependent. The repressive effect of TWA1 increases with rising temperatures, making it a key player in regulation of the chromatin interaction network under HS. This mechanism also assists plants in altering their physiological responses under HS, thus improving their persistence and productivity. Notably, Bohn et al. (2024) discovered that the inhibitory action of TWA1 is insignificant at 20°C but becomes significant at 25°C and even more obvious at 30°C. This temperature sensitivity highlights the role of TWA1 as a finely tuned thermosensor that can activate protective responses at critical temperature thresholds.Figure 1 Dynamic nature of the temperature-dependent regulatory mechanisms of the TWA1 thermosensor and potential implications for global agriculture.

(A) At baseline temperatures (20°C), TWA1 remains inactive and does not interact with JAM TFs or TPL co-repressors. Genes are expressed at basal levels, maintaining typical physiological functions under stress-free conditions.

(B) At high temperatures (30°C), TWA1 is activated by undergoing conformational changes, enabling it to interact substantially with JAM2 and TPL. These interactions result in the formation of an active repressor complex in nuclear subdomains. The highly variable region (HVR) of TWA1 plays a crucial role in sensing temperature shifts, enabling the thermosensory response. Formation of this complex leads to repression of ABA-responsive genes, thereby improving plant heat tolerance.

(C) Detailed interactions among TWA1, JAM2, and TPL in nuclear subdomains at high temperatures. The active form of TWA1 binds to JAM2 via its C-terminal portion and to TPL through its N-terminal domain through EAR motifs (thick yellow lines on TWA1). The HVR of TWA1 (thick black line on TWA1) is vital for these interactions, operating as a key thermosensory element. The repressor complex regulates gene expression by targeting G-box-related cis-elements as dimers, with TPL operating as a tetramer and interacting with Mediator complex subunits.

(D) The regulatory and thermosensory role of TWA1 in high-temperature responses includes the upregulation of HSFAs (e.g., HSFA2) and HSPs, essential elements that safeguard cellular proteins from denaturation and aggregation under high-temperature conditions. The interaction of TWA1 with JAM2 and TPL is important for maintenance of basal gene expression under stress-free conditions and triggering of stress tolerance mechanisms under high temperatures. Variation in the temperature thresholds of TWA1 orthologs, including AlTWA1 and SaTWA1, highlights the flexibility of this newly discovered thermosensor across diverse plant species. As shown by its variable temperature thresholds, this thermosensory mechanism has potential applications in the development of heat-smart agricultural strategies.

(E) By introducing TWA1 or its orthologs with required temperature thresholds into high-yielding crop varieties through traditional breeding (e.g., hybridization, marker-assisted breeding “selection or backcrossing”) or biotechnological methods (e.g., agrobacterium- or gene gun/biolistics-mediated transformation, or RNAi), we can design heat-smart cultivars that can thrive under climate change without compromising production.

(F) CRISPR–Cas-based gene editing can be used to induce or modify TWA1 genes in crop genomes, enabling specific control over their thermosensory responses and thus enhancing heat tolerance in the modified crops.

(G) The use of gene expression tools (e.g., (1) promoter engineering, including heat shock or tissue-specific promoters, (2) synthetic biology approaches, including gene switches or CRISPRa, and (3) epigenetic modifications such as DNA methylation editing or histone modification) to drive the expression of TWA1 under high temperatures can provide an adaptive benefit to crops, enabling them to react more efficiently and enhancing their high-temperature tolerance.

TWA1 homologs have been identified in both monocots and dicots, suggesting that the thermosensory role of TWA1 is conserved across diverse plant species. For instance, homologs from A. lyrata (AlTWA1) and Sinapis alba (SaTWA1) were shown to exhibit similar temperature-dependent regulatory functions, although with different temperature thresholds (Bohn et al., 2024). This phenomenon suggests that TWA1 and its orthologs can be exploited to design future heat-smart crop plants through breeding and biotechnological tools (Figures 1E–1G).

The discovery of TWA1 builds upon prior research on thermosensors in Arabidopsis. For example, diverse heat shock proteins (HSPs) and their co-chaperones were previously identified as essential components of the HS responses induced by regulating heat shock TFs. These HSPs protect cellular proteins from denaturation and aggregation under HS (Chen et al., 2014; Fragkostefanakis et al., 2015; Ding et al., 2020; Kang et al., 2022; Kan et al., 2023; Bohn et al., 2024; John et al., 2024). However, the discovery of TWA1 adds a new element by revealing a temperature-dependent regulatory mechanism that interacts directly with ABA-responsive pathways, offering a more integrative tool for HS management. Other thermosensors in Arabidopsis, such as phytochromes and the prion-like domain of ELF3, regulate thermally induced developmental adjustments such as flowering time and leaf morphology. For example, phytochromes function as thermosensors at night, integrating temperature information throughout the night to regulate gene expression (Jung et al., 2016). The prion-like domain of ELF3 has been characterized as a novel thermosensory mechanism that shifts rapidly between active and inactive states in response to temperature changes (Jung et al., 2020). In contrast to ELF3, TWA1 acts in the opposite way by repressing ABA-responsive gene expression under HS (Bohn et al., 2024). These discoveries highlight the complexity and diversity of plant thermosensory mechanisms and offer important insights for the development of new heat-smart agricultural strategies.

The mechanism by which TWA1 mediates transcriptional regulation and HS tolerance involves a complex network of protein–protein interactions and temperature-dependent conformational adjustments. Specifically, Bohn et al. (2024) confirmed that TWA1 interacts with JAM2 and TPL under HS, forming a repressor complex that prevents the expression of ABA-responsive genes (Figure 1). These interactions are also dependent on the subcellular localization of these proteins. The temperature-dependent nature of TWA1’s regulatory function arises mainly from its intrinsically disordered region, whose amino acid sequence is highly variable among orthologs. This variable region controls the temperature threshold for TWA1 activity, with individual orthologs demonstrating distinct temperature sensitivities. For example, AlTWA1 has a lower temperature threshold (IT50 of ∼20°C) than TWA1 (IT50 of 26°C) and SaTWA1 (IT50 of 30°C) (Bohn et al., 2024). This flexibility underlies the fine-tuned thermosensory responses in diverse plant species, mainly under HS. Moreover, by altering the expression of heat shock TFs and HSPs, TWA1 improves the plant’s ability to survive HS. This mechanism confirms that plants can immediately and efficiently respond to temperature shifts, thus retaining their physiological functions and promoting their survival under HS (Bohn et al., 2024).

Now the question arises of how exactly TWA1 coordinates the adjustment of ABA-responsive genes under HS. To address this, Bohn et al. (2024) demonstrated that the repressive effect of TWA1 on ABA-responsive gene expression is dose dependent and less pronounced in TWA1-deficient mutants (twa1-1 and twa1-2) than in wild-type Arabidopsis plants. These results indicate that TWA1 plays a vital role in maintaining basal gene expression levels under normal conditions and becomes more active under HS to increase stress tolerance.

Despite the breakthrough discovery of Bohn et al. (2024), further research is needed to fully harness the TWA1 regulatory network. For instance, it is unclear how TWA1 integrates signals from other stress pathways, such as ABA signaling in response to drought and salinity, and whether it cooperates with other TFs or co-repressors under specific stresses. The proposed role of post-translational modifications in the regulation of TWA1 activity and stability under HS also warrants further investigation.

The discovery and characterization of TWA1 have significant implications for global agriculture, specifically under a changing climate. By leveraging the thermosensory properties of TWA1, biotechnologists can design more heat-smart crops, guaranteeing better yields and food security (see Figure 1 for more discussion). The novel discovery of TWA1 not only provides a molecular tool for increasing HS tolerance but also raises new research questions. Understanding the detailed molecular mechanisms by which TWA1 interacts with JAM and TPL proteins and how these interactions are altered by HS could provide novel insights into plant stress responses. Investigating the potential crosstalk between TWA1-mediated signaling and other stress signaling pathways could offer new hope for increasing multi-stress tolerance in crop plants. Moreover, understanding the regulatory networks and downstream targets of TWA1 could shed light on the broader influence of thermosensors on plant stress biology. Harnessing the interaction between TWA1-mediated signaling and other phytohormone signaling pathways could lead to the discovery of new tools for the design of climate-smart crops.

Future investigations should also emphasize the environmental and ecological implications of implementing TWA1-based tools in agriculture. Evaluating the long-term effects of TWA1 expression on plant growth, development, and ecosystem interactions will be necessary to ensure the sustainability and security of these innovations. Finally, leveraging TWA1-type sensors will facilitate the design of heat-smart future crops, guaranteeing food security and agricultural sustainability for hot climatic regions. Several breeding and biotechnological tools can be used to achieve these goals, as detailed in Figures 1E–1G.

Funding

This work was supported by the Chinese National Key R&D Project for Synthetic Biology (2018YFA0902500 ), the National Natural Science Foundation of China (32273118 ), the Guangdong Key R&D Project (2022B1111070005 ), the Shenzhen Special Fund for Sustainable Development (KCXFZ20211020164013021 ), the Research Fund from Synthetic Biology Center of Shenzhen University, and the Shenzhen University 2035 Program for Excellent Research (2022B010 ) to Z.H.

Acknowledgments

We apologize to those whose work was not cited owing to space and reference number limitations. The figure was created with BioRender.com. No conflict of interest is declared.

Author contributions

A.R. and Z.H. conceived the idea. A.R. wrote the manuscript and prepared the figure. Q.U.Z. helped to improve an earlier version. Z.H. supervised, reviewed, and edited the manuscript. All authors read and approved the final version of the manuscript.

Published by the Plant Communications Shanghai Editorial Office in association with Cell Press, an imprint of Elsevier Inc., on behalf of CSPB and CEMPS, CAS.
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