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How tomato plants use their roots to ration water during drought

05/02/2024 - François-Xavier Branthôme
When water supplies are low, tomato roots produce suberin—the molecule that gives wine corks and waxy potato skins their water-repellant qualities—to control water flow.

Plants have to be flexible to survive environmental changes, and the adaptive methods they deploy must often be as changeable as the shifts in climate and condition to which they adapt. To cope with drought, plant roots produce a water-repellent polymer called suberin that blocks water from flowing up towards the leaves, where it would quickly evaporate. Without suberin, the resulting water loss would be like leaving the tap running.

In some plants, suberin is produced by endodermal cells that line the vessels inside the roots. But in others, like tomatoes, suberin is produced in exodermal cells that sit just below the skin of the root.

The role of exodermal suberin has long been unknown, but a new study by researchers at the University of California, Davis, published Jan. 2 in Nature Plants shows that it serves the same function as endodermal suberin, and that without it, tomato plants are less able to cope with water stress. This information could help scientists design drought-resistant crops.

 Alex Cantó-Pastor, a postdoctoral scholar working with Siobhan Brady, used mutant tomato plants to understand suberin’s role in drought tolerance. (TJ Ushing/UC Davis).  New work by Alex Cantó-Pastor (left) and Professor Siobhan Brady, Department of Plant Biology, shows how tomato plants protect themselves from drought by waterproofing their roots. The findings could lead to new ways to breed drought-tolerant tomato and other crops. (Photo by TJ Ushing for the College of Biological Sciences)

This adds exodermal suberin to our toolbox of ways to help plants survive for longer and cope with drought,” said Siobhan Brady, professor in the Department of Plant Biology and Genome Center and senior author on the paper. “It’s almost like a jigsaw puzzle—if you can figure out which cells have modifications that protect the plant during difficult environmental conditions, you can start to ask questions like, if you build those defenses up one upon the other, does it make the plant stronger?

In the new study, postdoctoral scholar Alex Cantó-Pastor worked with Brady and an international team of collaborators to uncover the role of exodermal suberin and map the genetic pathways that regulate its production.

Combining new and classical methods
It's really the merging of classical and cutting-edge methodology that lets us look at both the process that's happening in an individual cell and what you see in the whole plant,” said Brady. “So going from super small to really, really big.”

Brady, Cantó-Pastor and colleagues started by identifying all of the genes that are actively used by root exodermal cells. Then they performed gene editing to create mutant strains of tomato plant that lacked functional versions of several genes they suspected might be involved in suberin production. They discovered seven genes that were necessary for suberin deposition.  

Next, the researchers tested exodermal suberin's role in drought tolerance by exposing some of the mutant tomato plants to a ten-day drought. For these experiments, the researchers focused on two genes—SIASFT, an enzyme involved in suberin production and SlMYB92, a transcription factor that controls the expression of other genes involved in suberin production.

a, Graphical representation (left) of S. lycopersicum (cv. M82) root anatomy (the exodermis is highlighted in yellow) and representative cross-section (right) of a 7-day-old root stained with FY. Scale bar, 100 µm. b, Transmission electron microscopy cross-sections of 7-day-old roots obtained at 1 mm from the root–hypocotyl junction. Top: the epidermal (ep), exodermal (exo) and inner cortex (co) layers. Bottom: a close-up of the featured region (zone defined with blue dotted lines), showing the presence of suberin lamellae (SL). cw, cell wall; pm, plasma membrane. c, Fluorol yellow (FY) staining for suberin in wild-type 7-day-old plants treated with mock or 1 µM ABA for 48 h. Whole-mount staining of primary root (left) and mean fluorol yellow signal along the root (right), n = 6; error bars, s.d. Asterisks indicate significance with one-way analysis of variance (ANOVA) followed by a Tukey-Kramer post hoc test (***P < 0.005). NS, not significant. d, Developmental stages of suberin deposition of wild-type plants treated with mock or 1 µM ABA for 48 h. Zones were classified as non-suberized (white), patchy suberized (grey) and continuously suberized (yellow); letters indicate statistically different groups; apostrophes indicate different statistical comparisons; n = 6; error bars, s.d.

The experiments confirmed that both genes are necessary for suberin production, and that without them, tomato plants are less able to cope with water stress. The mutant plants grew as well as normal plants when they were well-watered but became significantly more wilted after ten days with no water. “In both of those cases where you have mutations in those genes, the plants are more stressed and they're not able to respond to drought conditions,” Brady said.

Having shown suberin’s worth in a greenhouse setting, the researchers now plan to test suberin’s drought-proofing potential in the field. “We’ve been working on taking this finding and putting it into the field to try and make tomatoes more drought tolerant,” Brady said.

Additional authors on the paper are: at UC Davis, Lidor Shaar-Moshe, Concepción Manzano, Sharon Gray, He Yang, Sana Mohammad, Niba Nirmal, G. Alex Mason, Mona Gouran, Kaisa Kajala, Kenneth A. Shackel, Donnelly A. West and Neelima Sinha; 
Prakash Timilsena and Song Li, Virginia Tech; 
Damien De Bellis, Robertas Ursache and Niko Geldner, University of Lausanne, Switzerland; 
Julia Holbein, Kiran Suresh and Rochus Benni Franke, Rheinische Friedrich-Wilhelms-University of Bonn, Germany; 
Alexander T. Borowsky and Julia Bailey-Serres, UC Riverside.,

The work was supported by the National Science Foundation and the Howard Hughes Medical Institute.

Some complementary data
Reference: Cantó-Pastor A, Kajala K, Shaar-Moshe L, et al. A suberized exodermis is required for tomato drought tolerance. Nat Plants. 2024
. doi: 10.1038/s41477-023-01567-x






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