NEW PAPER: The interplay of photosynthesis and evolution – resolving the anatomical paradox

Grantham Scholar Suma Mani explains the importance of a paper published today co-written by Suma’s supervisor Prof Colin Osborne (former Associate Directer of the Grantham Centre). The paper ‘C4 anatomy can evolve via a single developmental change can be read here

Photosynthesis is vital for life.

It removes carbon dioxide from the atmosphere to produce sugars. This process is powered by sunlight in specialised regions of the leaf called chloroplasts (chlorophyll containing organelles), which are found in the leaf tissue layers mesophyll and bundle sheath.

Photosynthesis is central to the functioning of any ecosystem because plants are the primary producers and source of energy for consumers.

Plants have successfully evolved to have two different photosynthetic pathways:

  • C3: where the first product of photosynthesis is a 3-carbon compound
  • C4: whose first product is a 4-carbon compound.

The striking difference between C3 and C4 plants is the presence of chloroplasts in bundle sheath cells in C4 plants, in addition to those in the mesophyll. This prevents the wasteful process of photorespiration, where oxygen gets fixed instead of carbon dioxide at higher temperatures.

While plants such as beans, wheat and potato use the C3 type of photosynthesis, sugarcane, corn, sorghum and millets are C4 plants.

C4 leaf of the grass Alloteropsis semialata indicating veins (dark-blue), bundle sheath cells (pale blue around the veins) and mesophyll cells (purple) (Image – Marjorie Lundgren)

Plants with C4 photosynthesis dominate the tropics and sub-tropics. Their evolution from C3 photosynthesis to a successful and highly efficient C4 pathway evolved more than 45 times in many families and appears to be an evolutionary wonder.

Like the many big questions surrounding human evolution, plants scientists have shown a great deal of interest in the evolution of plant traits. This is driven by a need to understand the diversity of plants and to evaluate whether there are any lessons out there for making our crops more productive. High yielding crops are important – to keep feeding people and to support rural economies.

A team of researchers from across the world have now unravelled how anatomical modifications in leaves have led to this transition over time and here I will try to explain their findings.

C3 and C4 photosynthesis: what are the differences?

Every plant on Earth uses the Calvin cycle for photosynthesis – a pathway in which the enzyme Rubisco fixes carbon dioxide that is dissolved from the atmosphere and diffused into the chloroplast. However, C4 plants utilize light energy to pump carbon dioxide into the chloroplasts within bundle sheath cells, thereby concentrating carbon dioxide around Rubisco and increasing photosynthetic efficiency.

Alloteropsis semialata (Image – Marjorie Lundgren)

The evolution of C4 plants is dates to around 30 million years ago, the early Oligocene period. This period was marked by increased oxygen concentrations and falling carbon dioxide concentrations in the atmosphere. Under conditions of decreased carbon dioxide availability, Rubisco’s affinity to fix oxygen negatively affected its functional efficiency.

As a counter-response, plants adapted to different photosynthetic pathways that increased Rubisco’s affinity to utilize carbon dioxide. The development of a new C4 pathway by anatomical modifications in the mesophyll and bundle sheath layers of leaf cells was crucial for evolution and survival.

In most C4 plants, the carbon pump works in mesophyll cells to deliver carbon dioxide at high concentrations in the bundle sheath where Rubisco is localized. To make this process efficient, evolutionary changes in anatomy have to increase the proportion of bundle sheath in the leaf. Since bundle sheath tissues are wrapped around veins, there are two ways this could happen – through the insertion of a greater number of veins or by bundle sheath cells around each vein becoming larger.

Alloteropsis semialata – the species that helped to solve the paradox

Alloteropsis semialata is unique among plants in having forms that use C4, C3 and intermediate (C3- C4) types of photosynthesis, widely distributed in tropical and subtropical areas of Africa, Australia and Asia. Commonly known as cockatoo grass in Australia and black seed grass in South Africa, the plant serves as a compelling model to discern the evolution of photosynthesis by comparing a continuum of leaf anatomy of each photosynthetic type ranging from C3 to C4.

In the southern African region of Zambia, these plants all coexist in the same geographic region with C4 forms that have also spread out across the Old-World tropics, as far as South East Asia and Australia.

Marjorie R. Lundgren, the lead-author of the paper, travelled extensively to Tanzania, Zambia, Australia, South Africa, Mozambique, Zimbabwe and Cameroon to collaborate with local botanists, and collect plant materials for the work in a highly international collaborative research effort. The team then quantified the anatomical changes in the leaf that accompanied the transition from non-C4 to C4 phenotypes. 

Alloteropsis semialata (image – Marjorie Lundgren)

Evolution of minor veins as a single developmental change

Marjorie and the other researchers tried to piece together what happened before the evolution of C4, what happened during the evolutionary event in C4 plants and what happened afterwards in some of the C4 plants. They reasoned that the traits that existed before the evolution of C4 will be shared by some of the non-C4 members, while those properties which took place subsequently as an adaptation will be restricted to C4 plants.

They found that C3, C3 – C4 and C4 Alloteropsis semialata have distinct leaf anatomy.

The only trait shared among all C4 individuals and none of the non-C4 plants is an increase in vein density, specifically minor vein development. The presence of minor veins in C4 plants increases the volume of bundle sheath cells in the leaf that boost the activity of Rubisco, distinguishing C4 plants. The presence of frequent and regularly spaced minor veins in the leaves is universally and uniquely associated with the C4 genome, which helps in establishing the overall anatomical variation between non- C4 and C4 phenotypes.

Professor Colin Osborne explains it this way: ‘C4 photosynthesis evolved by modifying the leaves of non-C4 species. However, most C4 plants are distantly related to non-C4 plants and have changed in a multitude of ways. The challenge for researchers is to get closer to the evolutionary transition from non-C4 to C4. Studying the huge variation within the Alloteropsis species lets us do this, to figure out what changed and when.’

The team successfully recognised the leaf features that differed consistently between C4 and non-C4 plants – the insertion of many small veins – which led to a leaf anatomy suitable for C4 photosynthesis.

The way forward

Lead-author (left) Marjorie Lundgren collecting samples at field (Image – Marjorie Lundgren)

The findings of this study have provided tremendous hope for engineering C4 photosynthesis in rice. Collaborative efforts between the International Rice Research Institute, Philippines, and various organizations across the world aim at introducing C4 traits into rice so as to increase the photosynthetic efficiency and boost rice production. This is achieved by manipulation of genetic, anatomical and biochemical traits guided by the C4 pathway. Armed with the knowledge about the developmental change needed, the team now hopes to start research on the genetic changes responsible for C4 anatomy.

With the global populations reaching an unprecedented high, food shortages are here to stay. This means a greater need for high yielding crops to ensure food security. A plausible approach to meet this need would be the introduction of C4 traits into rice to increase photosynthetic efficiency, thereby increasing crop yields which could help reduce world hunger.