Recently in Photosynthesis Category

In Darwinian Agriculture, I argued that accepting tradeoffs rejected by past natural selection is key to past and near-future crop improvement, whereas novel phenotypes never tested by natural selection may eventually make major contributions. In this post, I will briefly discuss two recent papers relevant to this hypothesis.

Lee DeHaan and David Van Tassel published "Useful insights from evolutionary biology for developing perennial grain crops", in American Journal of Botany, while Lin et al. published "A faster Rubisco with potential to increase photosynthesis in crops" in Nature.

Perennial plants often develop more extensive root systems than annuals, reducing the risk of erosion. Well-managed perennial forages (pastures and hay fields) are arguably our most-sustainable agricultural system, supplying milk, meat, wool, and leather, and often getting most of their nitrogen from symbiotic rhizobia bacteria (the main focus of my own research) rather than external inputs.

The Land Institute, where DeHaan and Van Tassel work, has been attempting to develop perennial grain crops. I have argued that greater investment of photosynthate or nitrogen in roots will usually leave less of these limiting resources for grain (seeds). All else being equal, DeHaan and Van Tassel apparently agree:

"where annual crops can use a similar amount of water, light, and nutrients as the perennials... annuals will indeed have greater yield potential"
But they have argued (and I agree, on p. 97 of my book) that perennials may sometimes capture more of these resources than annuals can. The last chapter of my book, on diversity and bet hedging, therefore included perennial grains as an example of high-risk approaches deserving some funding.

The potential of perennials to photosynthesize more months per year than annuals also implies using water more months per year, but their superior root systems can sometimes help water soak into the soil rather than being lost to runoff.

Actual results so far are somewhat discouraging, however. DeHaan and Van Tassel cite a paper by Culman et al., which found greater above-ground biomass in a perennial grass, kernza, relative to wheat. So it might be a better forage than wheat, but its grain yield (with moderate fertilizer) was only 4% that of wheat in year 1 and 39% in year 2. So it would take about 5 acres of kernza to produce as much grain as 1 acre of wheat. Where are those extra 4 acres (and the water to irrigate them) going to come from? Or can we realistically expect significant yield increases without losing the benefits of perenniality?

I have argued that while some tradeoffs (e.g., root vs. grain) constrain crop improvement, other tradeoffs can represent opportunities. For example, the fastest versions of the key photosynthetic enzyme work best at CO2 concentrations greater than atmospheric. Lin et al. transferred genes for one of these enzymes from cyanobacteria into tobacco. The resulting plants grew more slowly than unmodified tobacco, even at 9000 ppm CO2 (atmospheric is now 400 ppm). So this looks like a step in the wrong direction, but it's only a first step. The cyanobacterial enzyme works well in cyanobacteria because they also have a CO2-concentrating mechanism. Some plants, including corn, have different CO2-concentrating mechanisms. See "The evolutionary ecology of C4 plants" for an interesting discussion of how these mechanisms evolved in plants. If someone could combine the faster cyanobacterial enzyme with a plant or cyanobacterial concentrating mechanism, they might achieve significantly greater photosynthesis.

That could take a decade or more, but it's worth noting that perennial grains have been a significant focus of the Land Institute for most of their 38-year history.

There's probably some scientific connection between the two topics in this week's title, but I'm combining them because Ruben Milla has worked on both.

He and his colleagues just published a paper on "Shifts in stomatal traits following the domestication of plant species", comparing lots of crops with their wild relatives. Total abundance of stomata (leaf pores that let CO2 in and water vapor out) doesn't show a consistent increase or decrease with domestication, but there's a tendency for fewer of them to be on the lower side of the leaf.

In adding this paper to my database, I rediscovered one of Milla's earlier papers, on kin interactions in plants. Even though I'd blogged about it when it came out, I'd forgotten nearly all the details. I may be trying, unsuccessfully, to follow too many topics. Since some readers may have missed my earlier post, and since we are celebrating the 50th anniversary of Hamilton's and Maynard Smith's papers on inclusive fitness and kin selection, I am copying my 2009 post below.


This week I will discuss two papers, both dealing with plants and competition, in the context of genetic relatedness that might be expected to moderate competition:
"Growing with siblings: a common ground for cooperation or for fiercer competition among plants?" by Ruben Milla and colleagues (Proceedings of the Royal Society), and
"Do plant parts compete for resources? An evolutionary viewpoint" by Victor Sadras and me (New Phytologist).

Earlier I discussed a paper by Susan Dudley and Amanda File showing that some plants grow less root when interacting with related than with unrelated neighbors. Spending less resources on roots could have freed resources for more seed production, but they didn't measure that. Now Milla and colleagues have.
They grow three lupine plants per pot, using either three seeds from the same plant, three seeds from different plants in the same area, or three seeds from different parts of Spain, and measured various aspects of plant growth and reproduction. In contrast to what I might have expected from Dudley and File's work, plants surrounded by siblings produced no more seeds than plants surrounded by strangers. In fact, one of their measures showed significantly more seed production from plants growing with plants from other regions.

They suggest two possible explanations. First, there was some tendency for plants to grow taller when growing with close kin, perhaps because they all germinated at the same time and thereby triggered an "arms race" to get above each other. The resulting over-investment in stem could leave less resources for seed production. Their other explanation is almost the opposite. What if closely related plants invest less in root, as Dudley and File found, and (under the conditions of Milla's experiment) this resulted in too little root for optimal uptake of water and nutrients?

When wild plants are grown in pots in a greenhouse, they may not allocate resources optimally, nor respond normally to environmental cues, including cues about the relatedness of their neighbors. But if hypothetical cooperation among closely related plants is weak enough to be undermined (even reversed) by growth conditions, the tendency to cooperate can't be very strong.

I discussed a paper by Victor Sadras in one of my first posts in This Week in Evolution, so I was intrigued when he invited me to collaborate on a paper reviewing the idea of "competition" among parts of the same plant. We argue that mechanisms that look like within-plant competition often act to maximize overall plant reproduction. A branch shaded by another branch may die, but this is more like suicide than murder. We know this because the same degree of shading isn't lethal when the whole tree is shaded equally. When only one branch is shaded, however, it can increase the frequency of its genes in the next generation by sending its nitrogen to better-lit branches, where the photosynthesis rate per unit nitrogen is greater. Seeds produced on those branches carry the same genes as those that the shaded branch could have produced itself. Selfish genes lead to unselfish branches.

Competition among seeds on the same plant is a different story. These seeds may have different fathers, whose pollen contained competing versions of various genes. Gene variants that help a seed take more than its share of resources from the mother plant will tend to increase over generations, unless countered. But mother plants have various counter-measures that tend to equalize resources among seeds. (This contrasts with birds that can only bring enough food to feed one chick. They may lay two eggs, but then let the stronger chick kill the weaker.)

We suggested that natural selection for equalizing resources among seeds has often set limits on how much seeds can grow, even when conditions turn out to be unusually favorable during seed-fill. This tradeoff may have been worth it for genetically diverse wild plants. In modern agriculture, however, whole fields may be almost identical, genetically. We might therefore be able to eliminate some of these ancestral seed-balancing mechanisms, letting seeds grow more when conditions are good.

Such tradeoffs between past natural selection and present human goals are a major theme of my forthcoming book, "Darwinian Agriculture: where does Nature's wisdom lie?"

All five of my Darwinian Agriculture lectures at the International Rice Research Institute are now available on YouTube. My talks were prepared in advance, so I was only able to incorporate a small fraction of the interesting things I learned during my visit.

My last talk discussed the tendency (not necessarily by scientists themselves) to exaggerate research progress. For example:

"The researchers have already... successfully introduced 10 out of the 13 genes needed for C4 rice." -- Rice Today, January-March 2013, p. 5

Wheat, rice, soybean and tomato use C3 photosynthesis, named for the number of carbon atoms in the first product of photosynthesis. Maize ("corn" in the US) and sugar-cane use C4 photosynthesis. In hot climates, C4 photosynthesis can support higher rates of crop growth, using less water.

My book (p. 62) uses C4 photosynthesis as an example of "something that may have been easy for natural selection (given millions of years) [but] extremely difficult for humans." So I was surprised to learn, before arriving at IRRI, that C4 photosynthesis only needs 13 genes and that they have already transferred 10 of them. Maybe "skeptical" would be a better word.

I should have asked about this when I met with Paul Quick, who is leading the C4 rice project at IRRI. I'm guessing that he told the magazine that they've identified 13 key genes so far, and transferred 10 of them. My impression, from our discussions, is that they don't yet know the total number of genes they will need to transfer.

They have a lot of smart people, at IRRI and around the world, collaborating on C4 research. C4 rice will need :

* Some way to pump CO2 into bundle sheath cells around the leaf veins, from adjacent mesophyll cells.

* A diffusion barrier around the bundle sheath cells to keep the CO2 from leaking out again.

* More photosynthetic chloroplasts in the bundle sheath cells than rice has now.

* Ideally, closer vein spacing. The assumption is that CO2 can't be pumped very far, so if veins are widely spaced, only a fraction of the leaf will have C4 photosynthesis. But Paul Quick told me that corn husks have C4 photosynthesis throughout the leaf, despite widely-spaced veins. Interesting.

They seem to have made considerable progress on most of the above. I don't think he mentioned any progress on the diffusion barrier, though, which seems more critical than vein spacing, at least to me.
One of the clever approaches they are using is to knock out genes in a C4 plant, at random, to see which of them are essential to C4 photosynthesis. How do they tell if they've knocked out C4? Because of their CO2-concentrating mechanism, C4 plants can survive at much lower CO2 concentrations than C3 plants can. So they grow the random-knockout plant population at 15 ppm CO2 -- the atmosphere is 390 ppm and rising -- and look for plants that don't grow. Sounds like cruelty to plants, but they rescue them before they die, by transferring them to a high-CO2 tent. They're also drawing on IRRI's huge (100,000 genotype) collection of rice varieties and rice's wild relatives.

I don't know if they'll succeed, but this seems like a reasonable test of our current ability to improve complex traits in crops. At a minimum, they should get a lot of useful information about photosynthesis, leaf structure, the evolution of complex traits, etc. This information could have applications beyond improving photosynthesis. For example, the ability to develop crops with wider or narrower vein spacing would have applications in developing more-digestible crop leaves (for cows or for biofuel production). Vein spacing may also affect drought tolerance. Whether spending the same amount of money on other kinds of agricultural research would make more sense is a more-complex question. But the Gates Foundation is funding this "high-risk, high-potential-reward" research, so it doesn't come at the expense of their other work.

For more information, see IRRI's C4 rice page. For an interesting history of the project, see this video interview with John Sheehy, former head of the C4 rice project, who back visiting IRRI the same week I was there talking about Darwinian Agriculture.

Professor Peter Horton FRS called my attention to his blog post discussing some opportunities to improve crop photosynthesis and yield, in ways that were missed by past natural selection. He notes that:

"linking photosynthetic activity at the leaf level (the pre-occupation of the plant scientist) to crop yield per unit land area (the concern of the farmer) has proven very difficult."
Sometimes, there are tradeoffs between plant traits that maximize photosynthesis per unit leaf area and those that maximize photosynthesis by the community of crop plants. Thicker leaves (with more nitrogen per square cm) have higher photosynthesis rates per square cm. But, if a young plant doesn't yet have enough resources to completely shade the ground with thick leaves, making thick leaves means making too few leaves to intercept all the available sunlight. Photons that reach the soil without hitting a leaf don't contribute to photosynthesis. This tradeoff is among those discussed in a paper by Condon et al., (2004), cited and discussed in my book.

Professor Horton also suggests that:

"Put simply, stability and survival (a low risk strategy) in the natural environment are driving forces of evolution, not necessarily high growth rate and photosynthetic rate (a high risk strategy) or high grain yield."

Our major grain crops are all annuals, which produce seed and then die. But "survival" could mean "producing at least some seed that survive and grow in subsequent years." I agree that a plant strategy that almost always ensures that there will be some surviving offspring is probably not the plant strategy that maximizes good-year grain production.

What strategies work best for farmers -- and for society as a whole? A subsistence farmer might accept lower average yields, rather than risk occasional crop failures. A farmer in a market economy, though, might bank enough money most years to survive the occasional crop failure. This could be true even if the overall result of many farmers making that decision turns out to be greater risk of regional, or even global, food shortages.

But back to plants. Professor Horton closes with the suggestion that increased understanding of how optimization by natural selection may conflict with our goals for agriculture:

"may also be necessary to offset the inherent conservatism of plants that could thwart current attempts to increase photosynthetic efficiency, and hence yield"