Senescence is like a thermostat for the plant’s nitrogen (N) status – a nitrostat, I guess you could call it (but don’t get it mixed up the with nitroglycerin treatment for angina!).  Young growing tissues or developing storage organs have a large appetite for N.  If the need cannot be met through uptake of N by the roots, senescence will be triggered in older tissues and N assets will be mobilised.

The nitrostat is set at different levels of sensitivity in different species.  Some plants – particularly crop species, which have been bred to grab and use as much N as they can get – are nitrophiles (N-lovers) and have a very sensitive nitrostat.

If a grain crop like wheat or a green leafy vegetable like spinach doesn’t get the fertiliser it needs, its nitrostat is soon tripped and plants rapidly show signs of nutrient deficiency, which consist mainly of yellowing and the other symptoms of senescence.

This picture shows how dynamic the internal N economy of a cereal plant is during growth and ripening.  Notice how, from about 60 days, N is swept up into the developing maize grain from the rest of the shoot.

Other species are much less demanding and may even grow and develop poorly in high-N soils.  These are nitrophobes, and include many wild and endangered species – which is why eutrophication (over-fertilisation) endangers the biodiversity of many valuable natural habitats.

When the nitrostat kicks in, the proteins of older leaves begin to be converted to transportable forms of N which are relocated to areas of high demand in the plant.  For details of proteins and their structural units – amino acids – go here.

A champion N recycler is the burdock Arctium tomentosum.  During the second year of growth of this biennial monocarp, N is recycled three times, from tuber to rosette leaves and further to flower stem leaves, and eventually into seeds.

In green cells most of the mobilisable protein is in the plastid, and the two most abundant plastid proteins are rubisco (the enzyme that fixes CO₂) and LHCP, the chlorophyll-binding protein of the membrane complex that captures light energy for photosynthesis.

Rubisco is made of two subunits, one with a molecular weight of about 55000 and one of about 15000.  LHCP is actually a group of closely related proteins with a molecular weight of about 25000.  You can see these proteins quite prominently in leaf extracts separated by gel electrophoresis.

It’s clear that these proteins decline progressively as senescence proceeds.  New biochemistry that becomes active in senescence converts them into low molecular weight mobile products that are shipped out of the yellowing leaf to meet the N demands of tissues elsewhere in the plant.

The detailed enzymology and cell biology of protein breakdown in senescing plastids is an enduring mystery.  There are various ideas about what’s happening, and a fair amount of data that we hope in the end will make sense when put together in the right way – but we’re not there yet.

Enzymes that break down proteins into fragments (peptides) and individual amino acids are called peptidases.  What happens to make peptidases become active in senescence?

There are perhaps three possibilities.  One is that genes encoding peptidases, previously in the off state, are switched on during senescence and direct the synthesis of these enzymes from scratch.

It is certainly true that peptidase genes of various sorts are consistently identified amongst SAGs (senescence associated genes) from different species.  But there isn’t very much convincing evidence that the products of any of them ever normally come into contact with rubisco or LHCP in senescing cells.

Another suggestion is that the peptidases that break down plastid proteins are present in the cell before senescence starts, but are in an inactive form.  They have to become somehow unmasked as part of the senescence program before they can get to work on rubisco and LHCP.

This is an attractive idea because it resembles the mechanism of peptidase activation in apoptosis, a form of programmed death in the cells of animals and other organisms (maybe even plants).

In apoptosis there are cascades of activation in which sequential attacks by a chain of different peptidases are the activating events.  Some of the peptidases encoded by SAGs seem to resemble such activating peptidases.

Another possible mechanism for controlling protein breakdown in senescence is based on accessibility of protein substrates to peptidases.

There is good evidence from staygreen mutants that LHCP and other pigment-binding proteins are resistant to peptidase attack until chlorophyll is removed.  For this reason chlorophyll and protein breakdown in senescence are usually quite well coordinated.

Physical separation between peptidases and their substrates is another possible point of regulation.  Much of the peptidase activity in the cell (and many of the peptidases encoded by SAGs) are located in the cell vacuole, whereas the major mobilisable proteins are in the plastid.

Various mechanisms have been suggested for bringing vacuolar peptidases and plastid proteins into contact.  Recently researchers have described the presence of vesicles in senescing cells, either blebbing out from the plastid and carrying proteins to the vacuole for breakdown or else carrying vacuolar peptidases to the plastid.

I wouldn’t like to put my money on any one of the possible processes for breaking down plastid proteins at the moment; it may even turn out that all these mechanisms somehow combine to make N mobilisation happen.

The amino acids released by peptidase attack on plastid proteins usually undergo further metabolism before the N they carry is loaded into the plant’s transport system.

In particular, many plants seem to make amides such as glutamine and asparagine.  These compounds carry roughly twice as much N per unit carbon as most protein amino acids and may allow the senescing cell to salvage carbon skeletons for sustaining metabolism at a time when photosynthesis is declining.

The issue of N and carbon skeletons can have global implications, as a visit to this page will show.

You can read more about the fate of proteins in senescence in the following publications.

Dangl JL, Dietrich RA, Thomas H (2000) Senescence and programmed cell death. In: Biochemistry and Molecular Biology of Plants (eds B Buchanan, W Gruissem, R Jones) pp 1044-1100. Rockville: ASPP.

Feller U, Anders I, Mae T. 2007. Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. Journal of Experimental Botany doi:10.1093/jxb/erm242.

Heilmeier H, Schultze ED, Whale DM (1986) Carbon and nitrogen partitioning in the biennial monocarp Arctium tomentosum Mill. Oecologia 70: 466-474.

Masclaux C, Quillere I, Gallais A, Hirel B (2001) The challenge of remobilisation in plant nitrogen economy. A survey of physio-agronomic and molecular approaches. Annals of Applied Biology 138: 69-81.

Thomas H, Donnison I (2000) Back from the brink: plant senescence and its reversibility. In: Programmed Cell Death in Animals and Plants (eds J Bryant, S G Hughes, J M Garland) pp 149-162. Oxford: Bios.

Thomas H, Ougham H, Canter P, Donnison I (2002) What stay-green mutants tell us about nitrogen remobilisation in leaf senescence. Journal of Experimental Botany 53: 801-808.