Decoding tomato’s genetic defense against aluminum toxicity
image: A proposed model for possible roles of SlSTOP1-targeted genes in response to Al stress in tomato.
Credit: Horticulture Research
Aluminum toxicity is a major barrier to crop productivity in acidic soils, restricting root growth and nutrient uptake. Researchers have uncovered how tomato plants combat this stress through a genetic regulatory network. A key transcription factor, SlSTOP1, directly activates the potassium transporter gene SlHAK5, which in turn enhances citrate secretion from roots. Citrate binds toxic aluminum ions in the soil, reducing their harmful effects. Functional analysis of knockout lines confirmed that plants lacking these genes are hypersensitive to aluminum stress. This discovery highlights a novel genetic mechanism in tomato that could be exploited to breed crop varieties more resilient to soil acidity worldwide.
Acidic soils, which account for nearly 40% of global arable land, release soluble aluminum ions that rapidly inhibit root elongation, disrupt nutrient uptake, and cause yield losses of up to 80%. Plants employ two major strategies to tolerate aluminum stress: external exclusion of aluminum through root exudates and internal detoxification within cells. Among these, the secretion of organic acids such as citrate is one of the most effective external defense mechanisms. However, the regulatory pathways controlling this process remain poorly understood in tomato, a globally important vegetable crop sensitive to acidic soils. Due to these challenges, further investigation of tomato aluminum tolerance mechanisms is urgently
A research team from Yunnan Agricultural University, Zhejiang University, and Hangzhou Normal University published (DOI: 10.1093/hr/uhae282) their findings on October 2, 2024, in Horticulture Research. The study focused on uncovering the molecular basis of aluminum tolerance in tomato (Solanum lycopersicum). By combining genome-wide DNA affinity purification sequencing (DAP-seq) with RNA sequencing, the team identified SlSTOP1 as a master regulator of aluminum stress response. Crucially, they demonstrated that SlSTOP1 activates SlHAK5, a potassium transporter, to promote citrate secretion from roots, reducing aluminum accumulation in root tips.
The researchers first confirmed that SlSTOP1 is constitutively expressed in tomato roots and accumulates in the nucleus under aluminum stress. Knockout mutants lacking SlSTOP1 exhibited shortened roots, higher aluminum accumulation, and increased cell death compared to wild-type plants, underscoring its role in stress tolerance. Genome-wide binding analysis revealed 39 aluminum-responsive genes directly regulated by SlSTOP1, including transporters, transcription factors, and metabolic enzymes. Among these, SlHAK5 stood out as a direct target. Functional assays showed that SlHAK5 is localized to the plasma membrane and is essential for maintaining potassium nutrition. Importantly, CRISPR/Cas9-generated Slhak5 mutants were more sensitive to aluminum stress and secreted significantly less citrate than wild-type plants. Expression analyses demonstrated that SlHAK5 is specifically induced by aluminum but not by other metals or pH changes, and its induction occurs within 30 minutes of exposure. Supplementation with potassium improved citrate secretion and alleviated aluminum-induced root growth inhibition, linking potassium homeostasis to citrate-mediated detoxification. These findings reveal that the SlSTOP1–SlHAK5 module provides a crucial external exclusion mechanism by facilitating citrate release.
“Our study shows that SlSTOP1 directly controls SlHAK5, a gene previously known for potassium uptake, but now revealed to play a pivotal role in aluminum tolerance,” said Jianli Yang, senior author of the paper. “By linking potassium transport with citrate secretion, we uncovered a unique defense strategy in tomato roots. This not only deepens our understanding of plant adaptation to acidic soils but also opens new avenues for genetic improvement. Targeting the SlSTOP1–SlHAK5 regulatory pathway could accelerate the development of stress-resilient tomato cultivars.”
The discovery of the SlSTOP1–SlHAK5 regulatory pathway has broad agricultural significance. Tomato is among the most widely cultivated vegetables, yet its sensitivity to acidic soils limits production in many regions. By enhancing citrate secretion to neutralize aluminum, the identified mechanism offers a genetic basis for developing acid-tolerant tomato varieties through breeding or genome editing. Beyond tomato, the findings provide insights into how plants integrate ion transport and organic acid exudation to cope with soil toxicity. Applying this knowledge could improve crop productivity on acidic soils across Asia, Africa, and Latin America, where aluminum toxicity threatens food security.
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References
DOI
Original Source URL
https://doi.org/10.1093/hr/uhae282
Funding information
This work was financially supported by grants of the National Natural Science Foundation of China (32372803), and the Natural Science Foundation of Zhejiang Province (LZ22C150001).
About Horticulture Research
Horticulture Research is an open access journal of Nanjing Agricultural University and ranked number one in the Horticulture category of the Journal Citation Reports ™ from Clarivate, 2023. The journal is committed to publishing original research articles, reviews, perspectives, comments, correspondence articles and letters to the editor related to all major horticultural plants and disciplines, including biotechnology, breeding, cellular and molecular biology, evolution, genetics, inter-species interactions, physiology, and the origination and domestication of crops.