A billion-year-old conversation – plants’ internal dialogue
“Let us make a special effort to stop communicating with each other, so we can have some conversation.” Samuel Langhorne Clemens (Mark Twain) (1835-1910)
For hundreds of millions of years, plants have had an internal dialogue, and we are just beginning to learn the words. The dialogue occurs between two compartments within plant cells – the nucleus and the chloroplast. That dialogue has its genesis about one billion years ago. It’s a dialogue that continues today, shaping the productivity of the plants that support ecosystems, provide us with food, and determine the global carbon cycle.
By one billion years ago, evolution had forged tiny little cells that had the capacity to capture the energy from sunlight and use it to covert carbon dioxide and water into food – into sugars. That is, they were able to conduct photosynthesis. At the same time, much larger cells had evolved to eat in an entirely different way – they consumed other, smaller cells.
Over time, these two cell types came into contact with each other. At first, the large cells simply consumed the small cells. But evolution eventually equipped the small cells with the capacity to subvert the large cells’ digestive intent. Eventually, they were able to take up residence within their predators – churning out sugars for their new hosts in exchange for safety, security, and other resources.
The legacy of that simple merger is evident around us everyday. Plants carry the distant descendents of those original cells. Today, the descendents of the tiny photosynthetic cells exist as chloroplasts within the green tissues of the plants we see around us. Their long-term residence within plant cells has altered them. And it has also altered their long-time hosts.
Today, the fate of every plant cell is inextricably tied to the interaction between chloroplasts and other components of the plant cell. The most important of these interactions is with the nucleus.
The nucleus is the home of the genetic material for the plant – its genome. The genome contains all the genes a plant has, written in DNA code. Like us, plants have tens of thousands of genes in the nucleus.
Each gene encodes a specific set of instructions – like a recipe – for a particular cell component. The nucleus is like a non-circulating library for all the recipes a plant has. All the information is there, but it can’t leave the nucleus to be “cooked up” elsewhere in the cell. In order to use the information in the recipe library, it has to be transcribed into a different kind of information molecule – an RNA transcript. It is then transported out of the nucleus, where it can be used as instructions to create a particular piece of cellular machinery.
The nucleus contains genes that are recipes for cellular machinery needed for the chloroplast to do its job – to undertake photosynthesis. Consequently, it is important that the nucleus is instructed to transcribe these genes in response to appropriate cues. Key amongst these cues is light.
Light shapes the transcription of at least 20% of all plant genes. Light cues are perceived by receptors – specialised proteins that are activated by specific wavelengths of light – by different colours. Some respond to red light, others to blue light. When they are activated by light, these receptors travel to the nucleus where they direct the transcription of genes that provide recipes that are useful in the light. Some of these recipes are for parts of the chloroplast.
Surprisingly, some of the genes that are activated by light do not require these receptors. Instead, these genes are transcribed based on a signal that comes from the chloroplast. The chloroplast has “told” the nucleus that certain genes need to be transcribed. Signalling from the chloroplast to the nucleus is called retrograde signalling, and it has fascinated scientists for decades now, because the nature of the signal from the chloroplast is unknown.
Recently, this story became even more intriguing when it became evident that retrograde signalling did more than direct the transcription of genes – it directed the modification of the transcripts themselves. The transcripts are modified by splicing the RNA – removing bits of “superfluous” information from the transcript. This additional information needs to be removed from some RNA transcripts before they can exit the nucleus to be used in the cell.
Reporting in the journal Science, Ezequiel Petrillo, working in the laboratory of Alberto Kornblihtt, together with other colleagues, found a transcript that is differentially spliced in response to light, via retrograde signalling. The transcript in question encodes part of the cell’s splicing machinery, so the splicing process itself is regulated by a retrograde signal. Petrillo and colleagues found that the signal involved must be mobile. If they shone light on the leaves, cells in the roots contained the appropriately spliced transcript. If they removed the roots, which do not contain active chloroplasts, and shone light on them, the root cells did not contain the spliced transcript. This implies that the signal must travel from the aerial tissues to the roots – so that the entire plant body is informed that the leaves have perceived light.
So far, Petrillo and colleagues have ruled out sugar from photosynthesis as a signal. If sugars were provided to sugar-starved plants growing in the dark, the plants were unable to splice the transcript. So, it’s a novel signal that isn’t sugar, but the nature of that signal, and it gets to the nucleus within a given cell, let alone throughout the plant body is unknown. Other authors have suggested candidate retrograde signals involved in other aspects of chloroplast communication with the nucleus, but it remains to be seen if this signal is involved in the regulation of transcript splicing.
Chloroplasts have resided in cells with a nucleus for about a billion years now. That the chloroplasts have discovered ways of communicating to the nucleus is not entirely surprising. That they communicate using a mechanism that remains a mystery is fascinating. Learning the “words” of their language, such as the retrograde signal for splicing, will certainly drive intensive research for the coming years. Watch this space. It’s bound to be illuminating!
Images: All photographs by Malcolm M. Campbell.
Leister D (2012) Retrograde signaling in plants: from simple to complex scenarios. Frontiers in Plant Science 3:135
Petrillo et al. (2014) A chloroplast retrograde signal regulates nuclear alternative splicing. Science DOI: 10.1126/science.1250322
Woodson JD & Chory J (2012) Organelle signaling: How stressed chloroplasts communicate with the nucleus. Current Biology 22: 690-692