Heard it through the grapevine

11 October 2013 by Malcolm Campbell, posted in Biology

The sun, with all those planets revolving around it and dependent on it, can still ripen a bunch of grapes as if it had nothing else in the universe to do." Galileo Galilei (1564-1642)

The seasons have marched forward from summer to autumn. Harvest time is passing, and soon winter will be knocking on our door.

Human activity has tracked the change in seasons. In the field where the dogs and I play – we have shared it with all manner of sporting types for the past months – we virtually have the space to ourselves now.

Even if we were never to see people, the grape vine at the end of the field has marked the passing of the time for us. It was amongst the first plants to produce leaves in the spring. Leaves were followed not long after by the blossoming of compact, unassuming flowers, followed in turn by the emergence of grapes that ripened into tart purple fruit, which eventually were either eaten, fell to the ground, or withered, raisin-like, on the vine.

Grape vines follow this cycle year after year. They time leaf, flower and fruit production so as to match the availability of sunlight, water, pollinators, and disseminators of seeds. Evolution has honed grape vines so they track the prevailing conditions such that, at the end of the growing season, migratory birds and resident mammals can distribute the next generation of grape vines by consuming the fruit, and spreading its indigestible seed to new locales.

Grape vines simultaneously monitor temperature and day length to shape the timing of fruit production. Grape vines monitor day length, or photoperiod, using molecules that can detect light, photoreceptors known as phytochromes and cryptochromes. Phytochromes and cryptochromes can be thought of as switches, converted from an inactive to an active state, and then back again, depending on the quality of light that shines on the plant.

Phytochromes and cryptochromes contain a light-sensitive pigment, a chromophore, which is excited by particular wavelengths of light. This chromophore is attached to a protein. When the chromophore detects the appropriate wavelength of light, it induces a change in the structure of the protein. Other wavelengths of light cause the protein-chromophore complex to change back to its original shape. Phytochromes are responsive to light in the red wavelengths; whereas, cryptochromes are response to light in the blue wavelengths.

When light quality is appropriate, phytochrome and cryptochrome shape changes such that it is “active” – able to complete specific tasks. Specifically, active phytochromes and phytochromes invoke the activity of particular suites of genes. These suites of genes encode proteins that prepare the plant for sunlight – proteins involved in photosynthesis for example.

Crucially, phytochromes and cryptochromes also function to set plants’ circadian clock. As they are turned on and off by the presence of light, cryptochromes and phytochromes mark the start and conclusion of each day. This information is recorded by changes in gene activity. Amongst the genes that record this change are the pieces of an intricate molecular timekeeper, the circadian clock.

The circadian clock can be thought of as a timer that provides information to organisms about the day length they are experiencing, so that they undertake particular activities at appropriate times of the day or night. The day length measure provided to plants is also an important indicator of the season. Longer days correspond with the summer months – generally a time of the year when the plant should be growing, as well as engaged in fertilisation and ensuing seed production.

For the grape vine, its annual summer activities are informed by a combination of day length, provided by the circadian clock set by phytochromes and cryptochromes, together with warm temperatures. The mechanisms by which plants fine-tune their responses to critical temperatures is not well known, but it may occur by monitoring the efficiency of photosynthesis, by detecting the product of photosynthesis, sugar. The combination of a critical day length and a critical temperature are needed to instruct the plant to do two things: make leaves at the onset of spring, and then make flowers at the onset of summer.

Light and temperature information shape plant growth and development by acting on plant hormones.

We tend to think of hormones as a distinctly animal thing. Most of us are familiar with hormones like estrogen, testosterone, insulin, and growth hormone. Animal hormones are produced in one location in the body, and then act at a distant location to create a specific effect. Insulin, for example, is produced in the pancreas, and then acts on cells in the liver, fat tissue, and skeletal muscle to modulate glucose uptake.

Plants also make hormones. In fact, plants make a remarkable array of hormones – a vastly greater range of compounds than animals use as hormones. In addition, plant hormones work in ways that differ substantially from animal hormones. For instance, plant hormones can work within the cells where they are produced. In keeping with this, plant hormones can invoke their effect in a concentration-dependent manner – emanating from the cells in which they were produced. What’s more, as plant cells are directly connected with each other, plant hormones flow through the plant in a different manner than animal hormones are transported throughout the body. Finally, given the diversity of plant hormones, there is a remarkable potential for them to have interactive effects – that is, a hormone may act in different ways depending on what other hormones are being detected by the cell in question. This said, specific plant hormones tend to fulfil prominent roles during specific aspects of the plant life cycle.

In the late spring and early summer months, two plant hormones play a prominent role in the annual cycle of the grape vine. Auxins and gibberellins are produced in response to the rising temperature and longer day lengths. Auxins and gibberellins generally function to enhance elongation growth, particular that associated with emergence from a dormant state – like the bursting of buds to create leaves. Gibberellins are also involved in invoking flowering.

The conditions of early spring result in elevation of auxins and gibberellins in grape vines. In combination with sugar remobilised from the awakening stems and leaves, auxins and gibberellins promote the emergence of leaves. A mere 40-80 days later, provided the elevated temperatures persist, gibberellins promote flowering. It’s worth noting that there are literally scores of gibberellins that could be made by a given plant. Only certain gibberellins will promote flowering, and these are carefully synthesised at the appropriate time.

The small, relatively inconspicuous grape vine flowers are hermaphrodites. They bear both sexes – the female carpel and egg-producing ovule, and the male stamens with pollen-producing anthers. Pollination results in a little burst of auxin production, and then a big, sustained elevation of another plant hormone, brassinosteroid.

As their name implies, brassinosteroids are steroid hormones. Like animal anabolic steroid hormones, brassinosteroids give a boost to several facets of plant growth.  In grape vines, one of these facets is fruit production.

Brassinosteroids act by controlling the function of specific groups of genes. These genes encode proteins that increase sugar and water uptake in the fruit, as well as expansion of the cells that make up the skin and the flesh contained within.

As sugar levels rise within the fruit, two final plant hormones come into play. These two hormones are crucial in preparing the grape for its intended purpose – consumption. Up to this stage, the grape is a hard, green bulb of plant tissue. Not something that is particularly appealing as a foodstuff.

The grape vine is particularly adept at converting an unappetising bulb into the fruit that so many animals enjoy. Not surprisingly, this onset of the ripening process has garnered considerably human interest, particularly by those with an interest in using the grape for a purpose well beyond that intended by evolution – wine production. In keeping with this, the onset of grape ripening goes by an appropriately French name, véraison. Véraison involves the initiation of conversion of the hard, green-skinned fruit to a sugar-rich, purple- or yellow-skinned, soft-fleshed grape. Like the other processes in the annual cycle of the grape vine, véraison arises by a change in the functioning of specific suites of genes orchestrated by plant hormones.

Véraison is brought about by the combined action of two plant hormones, ethylene and abscisic acid.  Unlike the other plant hormones, ethylene and abscisic acid are not a collection of a class of chemicals, but rather two distinct chemicals.

Ethylene is a gas that seems to be necessary for véraison to occur. This was a surprising finding, as grapes have historically been thought of as plants that did not go through a climacteric ripening process involving ethylene. They were said to be non-climacteric fruit. While there is growing evidence for an essential role for ethylene in grape ripening, its precise mode of action is unknown so far.

By contrast, abscisic acid has a much better characterised role in véraison and the final stages of grape ripening.

In ripening grapes, abscisic acid is responsible for some of the critical events, including pigment production in the skin, the accumulation of sugars, and the loading of other nutrients in the flesh. Abscisic acid promotes these activities by enhancing the activity of some very specific genes, including one functioning as a switch for the pigment synthesis pathway.

In the final stage of the grape vine’s annual activity, abscisic acid lives up to its name. It enables abscission, the release of the fruit, to occur. Cells harden and degrade where the grape connects with the vine. The grapes drop where birds and other small animals can feed on them. Some will remain there uneaten – fertilising the ground with flesh, juice and skin – and releasing seeds to initiate the next generation of grape vines. Finally, abscisic acid induces the dormancy state for the vine itself – leaves drop off, hard buds are made to contend with the wintry conditions that will soon befall it.

Next spring it will all begin again.

There’s something comforting in that.

There’s something comforting in the knowledge that the grape vine keeps time with seasons. That it relies only on the fine-tuned machinery of evolution to orchestrate its annual trek through time. That its tempo is set by the motion and radiation of our home star relative to our planet.  That it persists, year-on-year, delivering a bounty that it shares with all takers, asking nothing more than some sunlight, warmth, and water.  In this time of thanksgiving, of celebrating Nature’s gifts, the grapevine is something worthy of gratitude.

References:

Chervin C, El-Kereamy A, Roustan JP, Latché A, Lamon J, & Bouzayen M (2004) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Science 167: 1301-1305

Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C,  & Cramer GR (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8: 429

Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, & Castellarin SD (2010) Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 232: 219-234

Halaly T, Pang X, Batikoff T, Crane O, Keren A, Venkateswari J, & Or E (2008) Similar mechanisms might be triggered by alternative external stimuli that induce dormancy release in grape buds. Planta, 228: 79-88

McClung CR (2006) Plant circadian rhythms. The Plant Cell 18: 792-803

Or E (2009) Grape Bud Dormancy Release − The Molecular Aspect. In Grapevine Molecular Physiology & Biotechnology (pp. 1-29). Springer Netherlands.

Pacey-Miller T, Scott, K, Ablett, E, Tingey, S, Ching, A , & Henry, R (2003) Genes associated with the end of dormancy in grapes. Functional & Integrative Genomics:144-152

Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB & Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiology 140: 150-158

Tesniere C, Pradal M, El-Kereamy A, Torregrosa L, Chatelet P, Roustan JP, & Chervin C (2004) Involvement of ethylene signalling in a non-climacteric fruit: new elements regarding the regulation of ADH expression in grapevine. Journal of Experimental Botany 55: 2235-2240

Wheeler S, Loveys B, Ford C, & Davies C (2009) The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. Australian Journal of Grape and Wine Research 15: 195-204

Ziliotto F, Corso M, Rizzini FM, Rasori A, Botton A, & Bonghi C (2012) Grape berry ripening delay induced by a pre-véraison NAA treatment is paralleled by a shift in the expression pattern of auxin-and ethylene-related genes. BMC Plant Biology 12: 185

Images: All photography by Malcolm M. Campbell

Dedication: This post is dedicated to the best partner a person could hope for, Joan Ouellette, on the day of our 27th wedding anniversary.

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2 Responses to “Heard it through the grapevine”

  1. Jim Woodgett Reply | Permalink

    As I enjoy a glass of wine tonight, I'll mourn the fate of the seeds lost to the next generation during the pressing process and toast biology for building such a tasteful process.

  2. Jim Woodgett Reply | Permalink

    As I enjoy a glass of prosecco tonight, I'll mourn the fate of the seeds lost to the next generation during the pressing process and toast the sun and biology for building such a tasteful process. Salut!

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