Selective Pressures And Evolutionary Dynamics In Hydraulic And Photosynthetic Systems Of The C3 And C4 Photosynthesis Pathways In Grasses

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Doctor of Philosophy (PhD)
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Biology
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C4 evolution
hydraulics
model
optimality
photosynthesis
physiological reorganization
Agricultural Science
Agriculture
Ecology and Evolutionary Biology
Evolution
Plant Sciences
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2019-10-23T20:19:00-07:00
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Abstract

It has generally been thought that the C4 photosynthetic pathway evolved from C3 ancestors due to low CO2 and high temperature, but recent studies have challenged this long-held hypothesis by suggesting water availability was a prime selective factor. Our work aimed to determine the importance and order that the environmental factors of CO2, temperature, water availability and light selected for C4 evolution and the evolutionary dynamics of hydraulics and photosynthesis traits along and after C4 evolution through time. First, we coupled hydraulics to photosynthesis models while optimizing photosynthesis over stomatal resistance and leaf/fine-root allocation to analyze the four selective pressures and their interactions through the historical origin and expansion of C4 plants. We found that water limitation was the primary driver for a C4 advantage with CO2 as high as 600 ppm in the Oligocene and low CO2 together with high light drove the mid-to-late Miocene global expansion of C4. Also, we predicted the geographical hotspots of C4 origins, consistent with fossil records, but the evolutionary center in northwest Africa and a Miocene-long origin in Australia are novel. Then, we analyzed the evolutionary divergence and reorganization of the hydraulic and photosynthesis system before and after C4 using mathematical models and phylogenetic comparative experiments for grasses. For hydraulic traits, C4 pathway led to higher hydraulic conductance (Kleaf), leaf capacitance (CFT) and leaf turgor loss point. The evolutionary trends of hydraulic traits diverged between C3 and C4: Kleaf and CFT decreased in C4 grasses, but not in C3; the evolution of C4 diminished the positive correlation between maximal assimilation rate and Kleaf. For photosynthesis traits, C4 have significantly higher resource allocation to light reaction than C3 and the empirical measurements are consistent with the optimal modeling. C4 have a significantly higher chlorophyll a/b and a significantly lower ratio of fluorescence-based electron transport, which indicated a lower proportion of linear electron transport. In addition, to analyze the divergence and evolution of the photosynthesis systems in C4, we extend the framework of widely-used estimation methods for C3 plants to build estimation tools of photosynthesis parameters for C4.

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Brent Helliker
Erol Akçay
Date of degree
2019-01-01
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