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[2013/01/07] Wilt Thou? Not with Guards in the Chem Lab
Wilt Thou? Not with Guards in the Chem Lab

Posted on January 7, 2013

Plants avoid wilting with pairs of guard cells performing chemical wizardry.

Leaves are peppered with oval pores called stomata (singular, stoma). Surrounding these pores are guard cells that control the rate of moisture escape and carbon dioxide intake. Under dry conditions, the guard cells relax and close the pores; when moisture is plentiful, they stiffen, opening the pore. But how do they do it? How do they “know” it’s dry, and what causes them to open the gates?

A new paper in Current Biology found something interesting: the guard cells know how to make abscisic acid (ABA*) from scratch. ABA is required to close the stoma. It’s remarkable that no one really figured this out till now, especially since Francis Darwin (Charles’s son), way back in 1898, observed stomata closing when the relative humidity (rh) drops. That observation was relatively simple; “however, our understanding of the signaling pathway responsible for coupling changes in rh to alterations in stomatal aperture is fragmentary.” Here’s what Bauer et al., a team of 14 mostly in Germany, found out by stressing plants with dry air and watching the genes that responded:

The results presented here highlight the primacy of abscisic acid (ABA) in the stomatal response to drying air. We show that guard cells possess the entire ABA biosynthesis pathway and that it appears upregulated by positive feedback by ABA. When wild-type Arabidopsis and the ABA-deficient mutant aba3-1 were exposed to reductions in rh, the aba3-1 mutant wilted, whereas the wild-type did not. However, when aba3-1 plants, in which ABA synthesis had been specifically rescued in guard cells, were challenged with dry air, they did not wilt. These data indicate that guard cell-autonomous ABA synthesis is required for and is sufficient for stomatal closure in response to low rh. Guard cell-autonomous ABA synthesis allows the plant to tailor leaf gas exchange exquisitely to suit the prevailing environmental conditions.

The team found 588 genes whose expression profiles changed when exposed to dry air. Of those, “131 belong to the class of guard cell-enriched genes,” they said. But that’s not all: “Within the pool of guard cell-expressed genes, 1,550 appeared sensitive to ABA, with 1,080 being upregulated and 470 being downregulated.” Within the cluster of robust ABA-induced genes, they found candidate genes that respond to humidity.

“One of the most striking features” of their observations was that guard cells contain all the genes necessary to synthesize abscisic acid. That’s not as easy as it looks. In their Figure 2A, they list 8 intermediate steps required to go from Beta-carotene to ABA, the first five steps taking place in the plastids of the guard cells, the last three in the cytosol.

Our results suggest that guard cells express the entire repertoire of ABA biosynthesis genes and that the abundance of their transcripts increases after exposure to ABA. This latter result suggests the existence of a positive feedback loop.

They further found that ABA is essential for stomal closure. Without it, leaves wilted. The leaves could be rescued, though, by turning on the ABA-expressing genes. In their final discussion you can sense their excitement at elucidating this elegant system:

Understanding how stomata respond to changes in atmospheric rh has been a key challenge since the phenomenon was first described by Francis Darwin. Our work and data from Okamoto et al. reveal a significant role for ABA in the stomatal response to both reduced and elevated rh. We also show that stomata are capable of responding to a reduction in rh in a cell-autonomous way, and this is mediated through the highly localized production of ABA.…

Guard cell-autonomous ABA synthesis not only allows an individual stoma to respond to changes in leaf hydration but also permits it to respond to changes in atmospheric rh and other stresses that use ABA as a signal. This in turn presents the plant with the possibility of exquisitely tuning leaf gas exchange to highly local environmental conditions. Furthermore, because our transcriptomic data are suggestive of a positive ABA-mediated feedback on ABA production, the possibilities for tightly controlled self-regulation at a highly local level over gas exchange are apparent. Our data add a new level of complexity to the overall understanding of how plants couple photosynthesis and water loss to changes in their environment.

The authors made no comment on how this “new level of complexity” arose by natural selection.

*The plant hormone ABA is also known as “(2Z,4E)-5-[(1S)-1-hydroxy-2,6,6-trimethyl-4-oxocyclohex-2-en-1-yl]-3-methylpenta-2,4-dienoic acid.” It has 15 carbons and 3 rings; its formula is C15H20O4. According to Wikipedia, “the C15 backbone of ABA is formed after cleavage of C40 carotenoids in MEP. Zeaxanthin is the first committed ABA precursor; a series of enzyme-catalyzed epoxidations and isomerizations via violaxanthin, and final cleavage of the C40 carotenoid by a dioxygenation reaction yields the proximal ABA precursor, xanthoxin, which is then further oxidized to ABA.” Abscisic acid, produced throughout the plant, is also involved in seed maturation, fruit ripening, leaf fall, photosynthesis rate, and salt stress. It can move rapidly throughout the plant in the xylem vessels.

Wonderful discovery; good experimental work by this team from Germany. If you want to know, here’s the recipe the guard cell has to know to cook up ABA (these things have to be synthesized in order): first, in the plastid, (1) beta-carotene, (2) zeazanthin, (3) antheraxanthin, (4) violaxanthin, (5) neoxanthin, (6) 9-cis violaxanthin; then, in the cytosol, (7) xanthoxin, (8) abscisic aldehyde, and finally (9) abscisic acid (ABA). That’s the “ABA Biosynthesis Pathway” involving at least 29 genes.

If old Frankie D. had known this earlier, he might have told Pop Charlie, “Hey dad, we have a problem. This natural selection thing doesn’t look like it can cut it with guard cells. They’re a LOT more complicated than we thought. Maybe you should stop making like a phylogenetic tree, and leaf.”



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