Changes in How a Plant Breathes Aren’t Always Matched by Changes in Its Anatomy

Plants can breathe, or at least respire, in a few different ways. There are advantages and disadvantages to the different methods. But how does a plant shift from one method to another? Katherine Heyduk and colleagues have been finding out with the help of Yucca gloriosa, a hybrid found in the southeast of the USA that switches between two different methods.

Typically a plant uses a process called C₃ photosynthesis to convert carbon dioxide and water to glucose. Usually it works well enough, but in hotter and drier climates instead of capturing carbon dioxide, the plant captures oxygen and ends up losing energy. CAM photosynthesis is a method some plants use to collect carbon dioxide at night and temporarily store it as an acid. During the day, stomata close, to prevent water loss, and the acid is turned back to carbon dioxide and sent to the chloroplasts to turn to glucose.

CAM photosynthesis can help conserve water in a plant as it closes the plant stomata during the heat of the day, reducing water loss. However, it has drawbacks as it uses energy shuttling the carbon molecules around the leaf. But a plant doesn’t have to choose to use just one method or another, Heyduk and colleagues write. “Since all CAM plants retain and use the entire C₃ machinery, many species fix carbon through a mixture of both pathways. Strong CAM plants use CAM for the vast majority of their carbon uptake, while C₃+CAM species use a mix of both pathways to fix CO₂… Moreover, plants can vary not only in their ability to use CAM, but also the degree to which CAM can be modulated under abiotic stress.”

Yet C₃ and CAM have different ways of working, so how is this reflected in the anatomy of the plant? The team examined Yucca gloriosa, Spanish Dagger, a wild cross between Y. aloifolia, a CAM species and Y. filamentosa, a C₃ species. You can find it growing in a narrow strip on near the coast between Florida and Virginia. Usefully, it is happy using both methods of photosynthesis. What the scientists wanted to know was if there was genetic variation in how the plants used CAM photosynthesis. If there was, was there also a corresponding anatomical difference?

The experiment started by collecting plants between Florida and Virginia as ramets, offshoots from a plant. They were taken back to the University of Georgia and grown in the same greenhouse. After six months, once the team was sure that the plants were growing properly, they started dividing them into groups for experiments in drought response.

What they found was CAM photosynthesis was upregulated in drought, but the plant’s genes had an influence on how well they could do that. But there wasn’t a simple tale of genetic difference.

“Detailed physiological and anatomical measurements in Y. gloriosa have revealed among-genotype variation in CAM phenotypes, and that anatomical and physiological traits show a lack of correlation within Y. gloriosa,” write Heyduk and colleagues. “Under drought stress, the levels of daytime CO₂ assimilation were largely driven by environment—that is, soil moisture content— whereas nocturnal CO₂ assimilation rates and acid accumulation were influenced by a combination of genotype and environmental effects. Our results reveal a continuum of photosynthetic traits across Y. gloriosa genotypes, including variation in drought response. Anatomical measurements were largely not predictive of physiological traits within Y. gloriosa.”

“In contrast, cell size, IAS [Intercellular airspace], and leaf thickness were predictive of nocturnal CO₂ uptake in cross species comparisons. These observations suggest that anatomical characteristics can be decoupled from photosynthetic physiology of CAM within the homoploid hybrid species Y. gloriosa.”

“The lack of correlation within the intermediate Y. gloriosa suggests that the evolutionary trajectory to CAM from C3 passes through a stage where many combinations of anatomical and photosynthetic physiology traits are viable.”