What a tree does with light

Imagine a photon leaving the Sun's bright surface, bound for a forest in Costa Rica. A photon carries a discrete amount, or packet, of energy; ours is a photon of red light. It crosses space and, about eight minutes and twenty seconds later, slips through Earth's atmosphere. Below, a breeze turns a leaf near the top of a crown, then lets it settle in the sun. Our photon strikes the leaf's surface.

It arrives among an immense stream of photons. Hold your palm toward strong midday sun: over an area of 100 square centimeters, roughly 40 billion billion photons arrive each second, including invisible ultraviolet and infrared light. At ground level, infrared carries slightly more energy than visible light; ultraviolet contributes much less. Our eyes detect a band of photon energies as colors, from red at the lower-energy end to violet at the higher-energy end. Infrared photons carry less energy than visible red photons; ultraviolet photons carry more than visible violet photons. Both fall outside the range our eyes can see.

Let's follow our red photon into a leaf cell and toward one of its chloroplasts, the small green compartments where photosynthesis uses sunlight to make sugars. The chloroplast's two outer membranes let visible light through. Beyond them, flattened sacs lie in watery fluid, many stacked like coins and linked by membrane bridges. Their connected interiors hold water and dissolved substances within thin membrane walls. Proteins embedded in these walls hold chlorophyll and other pigment molecules in light-collecting clusters called photosystems. (A pigment is a substance that gives something its color by absorbing some colors of visible light more strongly than others.) Each of the many photosystems gathers energy for a single reaction center, also held in the membrane, where that energy can start electron transfer. Sugar-building enzymes occupy the fluid around the sacs.

Our red photon meets a light-collecting chlorophyll molecule held by a protein embedded in the sac's membrane wall. The chlorophyll absorbs our photon, taking all its energy and lifting one of chlorophyll's electrons into a higher energy state. The photon ceases to exist; the energy it carried across space in the electric and magnetic fields of light now resides in the excited molecule.

Our photon's energy now passes between neighboring pigment molecules in the membrane. (Note to readers: we're going to deep dive into the chemistry for a few paragraphs. If this gets too heavy for you, skip down to after the next image.) Through electrical interactions, an electron in one molecule drops to a lower energy state as an electron in its neighbor rises. At this stage in the process, pigment molecules pass energy to one another without exchanging electrons. Along the way, energy can leak away as heat or escape in a newly emitted photon, the leaf's faint fluorescence, too weak to observe in daylight with the naked eye. When excitation arrives at the photosystem's reaction center, still within the membrane, a chlorophyll molecule there passes an electron to a pheophytin molecule (another type of pigment, similar to chlorophyll except that it lacks magnesium). The pheophytin molecule gains a negative charge by accepting the electron, while the chlorophyll molecule becomes positively charged (remaining positively charged until an electron supplied from water restores its neutrality). From the pheophytin molecule, the electron passes in turn through two quinone molecules, fat-soluble carriers held in the photosystem. The second quinone collects the electron we are following and another sent along the same route using energy from a second photon. Once it has both, it travels through the membrane to cytochrome b6f, an iron-containing protein complex anchored there. Cytochrome b6f passes electrons to a copper-containing protein in the fluid inside the sacs. The carriers' differing attraction for electrons favors these successive handoffs, releasing energy as the electrons move toward lower energy states.

Our photon has supplied energy to photosystem II, the first of two kinds of light-collecting assembly that work in sequence. Each time its reaction center sends an electron onward, it needs a replacement. On the membrane's inner face, a protein complex containing manganese and calcium uses the energy captured by photosystem II to draw replacement electrons from water in the sac. To release one molecule of oxygen gas, the complex must split two water molecules: each water molecule supplies one of the two oxygen atoms joined in the oxygen molecule. Each time photosystem II absorbs another photon and its reaction center sends an electron onward, the complex supplies a replacement electron from water. After four such transfers, the two water molecules have yielded four electrons, four positively charged hydrogen ions and one oxygen molecule. (These products account for every atom in the original water molecules, with no other residue. The oxygen can escape from the leaf, while the hydrogen ions collect inside the sac.)

Cytochrome b6f uses energy released by the electrons excited by sunlight to pump hydrogen ions from the chloroplast fluid outside the sacs into their interiors, adding to the ions released from water. As ions accumulate, their buildup drives them back into the fluid outside the sacs through ATP synthase, an enzyme spanning the membrane. Their flow powers the enzyme to assemble ATP, adenosine triphosphate, which supplies energy for building sugars. (The ingredients are already dissolved in the fluid outside the sacs: ADP, a molecule the cell makes and reuses, and phosphate, a nutrient containing phosphorus absorbed by the roots. ADP bears two phosphate groups; the enzyme adds one more to make ATP's three.)

The copper-containing protein that receives electrons from Cytochrome b6f carries them through the fluid inside the sacs to photosystem I, also embedded in the membrane. Having given up energy for ATP production, the electrons need a second boost to supply the sugar-building reactions. Photosystem I's own pigments absorb other photons and deliver their energy to its reaction center, which raises the electrons' energy again. A small iron-containing protein brings the newly energized electrons, one at a time, to an enzyme in the fluid outside the sacs. The enzyme binds this protein and NADP+, a molecule the cell makes and reuses, allowing electrons to pass to NADP+, where they are more tightly bound. Two electrons and a hydrogen ion from this fluid produce NADPH, which carries electrons to the sugar-building enzymes nearby. Those enzymes use ATP's energy and NADPH's electrons, returning ADP, phosphate and NADP+ to the chloroplast fluid outside the sacs for the light-driven reactions to turn into fresh ATP and NADPH.

With ATP and NADPH supplying energy and electrons, the leaf also needs carbon to make sugars, and ultimately new tissue. It draws that carbon from carbon dioxide in the air. Each carbon dioxide molecule contains one carbon atom joined to two oxygen atoms, and the whole molecule can enter through a pore called a stoma. Entry is passive: gas molecules move randomly in both directions through an open pore. As photosynthesis consumes carbon dioxide inside the leaf, the lower concentration there means more molecules enter than leave. This net movement is diffusion. Wind mixes and replenishes the air near the leaf's surface, helping carbon dioxide reach the pores.

Oxygen and nitrogen molecules can pass through the same opening: the pore does not sort the gases. Once inside, oxygen can dissolve in moisture and enter cells, where it is used in respiration to release energy from sugars. Oxygen molecules can diffuse back out, too, along with oxygen produced by photosynthesis. Nitrogen gas mostly remains unreacted and can leave again: leaf cells cannot directly use it to make their nitrogen-containing compounds.

To reach a chloroplast, carbon dioxide moves through a network of microscopic, air-filled gaps between the leaf's cells. These connected spaces expose the cells' moist walls to the gases entering through the pores. Carbon dioxide dissolves in that moisture and passes into the cells, reaching the fluid around the chloroplasts' internal membrane sacs.

There, an enzyme attaches carbon dioxide to a carbon compound already present. The resulting molecule splits into smaller compounds, which further reactions transform using ATP's energy and NADPH's electrons. These products are small molecules with three carbon atoms. Some supply raw material for sugars; the rest regenerate the compound that accepts incoming carbon dioxide, allowing the cycle to continue.

In Physiology of Woody Plants, Stephen G. Pallardy follows these products into transport, storage and construction. Some of these sugar-building molecules leave the chloroplast and are converted into sucrose elsewhere in the cell; others become starch stored within the chloroplast. The leaf exports sucrose through the phloem, the sugar-conducting tissue in leaf veins and beneath the bark, to other parts of the tree. In growing tissues, sugars supply material for wood, roots and leaves. Pallardy describes how enzymes join glucose units into long cellulose chains, which form strong fibers in cell walls. Carbon that entered the leaf from the air can thus become part of a new wood cell.

That contribution from the air is substantial. Adam Martin and Sean Thomas measured wood from 59 Panamanian rainforest tree species and found that carbon accounted for an average of 47.4 percent of its dry mass, the mass excluding water. Trees acquire that carbon through photosynthesis. Most of the remaining dry wood consists of oxygen and hydrogen, supplied through carbon dioxide and water. Roots provide the water as well as mineral nutrients, which contribute a much smaller share of dry wood. A trunk is therefore built largely from carbon dioxide and water, with sunlight supplying the energy to assemble its substance.

Building and maintaining that wood also consumes some of the sugars the leaf makes. The tree breaks them down through respiration to release energy for construction and upkeep. A leaf in the sun supplies both material and fuel for growth.

You might expect bigger trees with more leaves in the sun to add more wood. But does wood production rise in proportion to the light they capture? Between the light striking a crown and the thickening of its trunk, leaves must acquire carbon and the tree must divide it among competing uses. A stem measurement alone cannot tell us whether slow growth reflects a shortage of carbon or a greater share going elsewhere.

In Japanese forest plots, taller trees generally captured more light for their aboveground mass yet tended to add less new mass per unit of light. But at 4 Brazilian eucalyptus sites, Dan Binkley's team found that larger trees produced more stem mass per unit of light. The Brazilian result fits a common pattern in wood-production studies: a 2013 synthesis by Binkley and colleagues found that larger trees often made more wood per unit of absorbed light. Yusuke Onoda's Japanese comparisons pooled different species, including trees adapted to shade; within several species, taller individuals also grew more per unit of light. The studies measured different tissues under different conditions, so neither pattern is a rule for every forest.

More wood from nearly the same light

Michael Ryan's team, studying the same 4 Brazilian plantation sites, wanted to understand how water availability affects wood growth. They supplied extra water to some stands and compared them with stands receiving only rainfall. Irrigated stands produced 27 percent more wood than unirrigated stands, while absorbing an estimated 5 percent more light. The team reported the experiment in 2010 alongside Binkley's individual-tree analysis.

A shortage of water can limit both a leaf's carbon uptake and the growth that uses the sugars the leaf produces. The pores that admit carbon dioxide also lose water vapor; closing them conserves water at the expense of carbon uptake, even in bright sun. Having sugar on hand isn't enough. Growing cells also need water to expand. Pallardy, writing in Physiology of Woody Plants, describes both constraints. Irrigation can relieve constraints at different stages, which is why a light reading alone cannot predict the resulting growth.

The stomata through which we followed carbon dioxide into the leaf can change width: each is flanked by two guard cells. To open a pore, these cells take up mineral ions, especially potassium supplied from the soil by the roots. The ions and sugars accumulating inside draw in water, swelling the cells so they bend apart. This control over carbon entry is one way the leaf regulates sugar production; the tree's ability to use those sugars matters too. Pallardy describes how photosynthesis can slow when sugar use, storage and export cannot keep pace with production. Growing roots and shoots help sustain demand. We usually imagine leaves supplying growth, but the capacity to grow can influence how much carbon the leaves acquire.

In the Brazilian experiment, Ryan's team estimated that irrigated stands acquired 18 percent more carbon through photosynthesis than unirrigated stands and put a greater share of it into wood. They worked backward from where the carbon went: into new wood and foliage, belowground, or back into the air as aboveground tissues broke down sugars for energy through respiration. Some estimates depended on respiration measurements extrapolated beyond the trees and dates sampled. The estimates leave less certainty about how much of the extra wood came from increased carbon uptake and how much from altered carbon use.

Even with adequate water, pouring more light onto an already bright leaf eventually brings little additional carbon uptake. Photosynthetic capacity has limits, partly set by the supply of nitrogen-rich proteins that transfer electrons and help turn carbon dioxide into sugars. Light reaching a shaded leaf can therefore be more useful than the same addition to a leaf already near its limit. In other words, a plant's carbon uptake can depend on where its leaves sit in the light as well as how much leaf area it exposes.

An experiment with sunflowers tested whether letting plants change that arrangement could increase their yield. In dense, irrigated and fertilized stands in Buenos Aires, Mónica López Pereira's team held some stems upright with wire frames. Others could lean to alternating sides of their rows, spreading their foliage outward. At the same planting densities, the freely inclining stands produced 19–47 percent more seed oil. Changing the position of stems and leaves had changed production within the same planted area.

Under a forest canopy, a leaf's carbon uptake also depends on when direct sunlight reaches it and how long it lasts. A patch of sun may cross a leaf and disappear before its photosynthetic enzymes and pores have fully responded to the brighter light. After one such sunfleck, enzymes can remain active and pores can remain open, allowing the leaf to acquire carbon more quickly during the next pulse. So equal daily light totals can yield different carbon gains depending on the spacing of those pulses.

A lasting change from shade to sun requires a longer adjustment. A plant grown in a pot under shade can develop bleached or brown, scorched patches if moved straight into strong sunlight. Gardeners reduce that risk by gradually increasing its sun exposure, part of the process called hardening off. The University of Maryland Extension recommends starting seedlings in a sheltered, shaded place and increasing sunlight each day. That preparation suits plants destined for sunnier conditions; a species adapted to shade may still struggle in full sun.

When a large canopy tree falls, the plants beneath it get no gradual introduction: leaves accustomed to shade can suddenly face hours of direct sun. They may absorb more energy than their photosynthetic reactions can use, and carbon uptake can initially fall despite the extra light. Leaves can adjust their pigments and release more excess energy as heat, but species differ in how well they cope. In simulated tree-fall gaps in Panama, G. Heinrich Krause and colleagues found that pioneer seedlings recovered photosystem efficiency more fully after sun exposure than the late-succession seedlings tested. An opening creates room for growth while exposing the existing understory to a period of light stress.

The carbon that does not become wood

To follow the carbon acquired with sunlight into new wood, we first need to know how much enters the tree. A gas-exchange chamber can measure a leaf's carbon dioxide uptake during a brief test. To estimate a tree's carbon uptake over a year, researchers need to know how much foliage it carries, where light falls within its crown and what conditions its leaves experience. The same amount of intercepted sunlight can yield different amounts of carbon because water supply, leaf position and the timing of illumination affect uptake. Putting that estimate beside measured wood growth lets us test whether trees that acquire more carbon also make proportionately more wood.

Ezequiel Fernandez-Tschieder and colleagues made that comparison in a eucalyptus plantation at Mogi Guaçu, Brazil. They followed 18 genetically identical trees of the same age for eighteen months: 6 dominant trees, 6 of intermediate size and 6 suppressed neighbors growing beneath others. The dominant trees acquired an estimated 35 percent more carbon, yet produced nearly three times as much wood. Their greater carbon uptake could explain only part of their greater wood production. They also put a larger share into wood: 25 percent of their estimated photosynthetic carbon uptake, compared with 12 percent in suppressed trees.

Where did the rest go? The team estimated that suppressed trees sent 58 percent of their carbon belowground, compared with 27 percent in dominant trees. The absolute amounts did not differ significantly: a similar amount took a larger fraction of the smaller trees' supply. To estimate those amounts, the team measured water flow through the trunks and sampled sugars beneath the bark on 4 dates. The sugars' carbon-isotope composition helped estimate carbon uptake per unit of water used; combining that estimate with water flow gave an estimate of photosynthesis. They then subtracted the carbon used for aboveground growth and the amount attributed to respiration by their model, leaving an estimate of the carbon available for belowground uses. The estimate includes carbon used in root growth and respiration, released by roots or supplied to fungi; the team did not measure each use separately. Fernandez-Tschieder and colleagues concluded that carbon allocation explained most of the dominant trees' advantage in wood production per unit of water used. That budget does not reveal how much carbon accumulated as reserves, or whether those reserves could support a burst of upward growth after a canopy opening.

Reaching brighter light requires functioning roots as well as a taller stem: roots supply the water and nutrients needed to build and sustain new foliage. A shaded plant also has to survive periods when its leaves cannot cover its carbon needs. In Panama, Jonathan Myers and Kaoru Kitajima tested seedlings of seven woody species by removing their leaves or placing them in deeper shade. Species with larger initial stores of carbohydrates in stems and roots survived better, and those stores declined during the treatments. Larger reserves were also associated with better leaf replacement after defoliation. Stored sugars and starch could keep these seedlings alive through setbacks, helping them persist until growing conditions improved.

Even when a canopy opening arrives, added light need not produce an immediate surge in height. Shawna Naidu and Evan DeLucia moved potted red-oak saplings from forest shade into a gap after their leaves had developed. During that growing season, the saplings added roots, thickened their stems and accumulated carbohydrate reserves, but did not grow taller. The researchers suggested that the larger reserves could support a stronger flush of growth the following year; however, they did not measure that next year's response. The added light had supported roots and reserves without an immediate gain in height.

It's worth keeping in mind that a tree can grow new leaves without increasing the mass of foliage in its crown: new leaves replace those that fall. Flowers, fruit and seeds also leave the crown, while fine roots grow and die belowground. A tree may therefore produce tissue and sustain its existing body while adding little to its trunk. Wrap a tape measure around the trunk and you miss both that production and the reserves that may support later growth.

The living cells in existing wood need sugars too. As a tree grows larger, could its living wood cells consume so much carbon to stay alive that less remains for new wood? Michael Ryan and colleagues tested that explanation in Hawaiian plantations of Eucalyptus saligna, where annual wood production peaked when neighboring crowns met, then fell as the stands aged. The trees kept accumulating wood, but added less each year.

The team measured how much carbon living wood cells consumed through respiration, the process of breaking down sugars to release energy. That consumption fell as the stands aged. Increasing wood respiration therefore could not explain why the trees were producing less new wood.

To estimate how much carbon the leaves acquired through photosynthesis, the researchers added up the carbon used aboveground for growth and respiration or sent belowground. Between ages two and six, the trees' estimated annual carbon uptake fell by about a third. Of the carbon the leaves acquired, a greater share went belowground and a greater share was consumed in leaf respiration, leaving a smaller share for new wood. With less carbon coming in and a smaller share becoming wood, annual wood production fell by more than half. The study did not establish why the leaves acquired less carbon.

Sunlight supplies the energy for leaves to turn carbon dioxide into sugars. The tree uses those sugars to build wood, sustain living cells, replace leaves and build up reserves. How much wood it adds depends both on the carbon its leaves acquire and on how much goes to those other uses. What allows a tree to stay alive for years in the shade while adding little new wood? We'll investigate this next...