Long-lived photosynthesis: Five decades of photosynthetic activity and foliar senescence in the needles of Pinus longaeva in California's White Mountains

Background/Question/Methods

Pinus longaeva (Great Basin bristlecone pine), high in California's White Mountains, holds the record for oldest unitary plant, is a classic example of whole-plant negligible senescence, and produces the earth's longest-lived photosynthetic foliar tissues. Some individuals of this species retain living needles for up to 49 years, one to two orders of magnitude longer than most vascular plant species. Bristlecone growth patterns allow annually resolved aging of needles on selected branches, thereby permitting assessments of photosynthesis in foliage of known ages. We studied photosynthetic function in different aged needles of P. longaeva to examine needle-level photosynthetic senescence, asking two key questions: First, are patterns of photosynthetic senescence in this exceptionally long-lived foliage qualitatively different from patterns in other vascular plant species? Secondly, how do mechanisms of photosynthetic senescence in these needles compare to that of foliage in other vascular plant species?  Measurements included photosynthetic CO₂ assimilation on discretely aged clumps of needles, photosynthetic O₂ production and chlorophyll fluorescence on individual needles, as well as assessments of needle nitrogen (N_L) and chlorophyll (chl).

Results/Conclusions

Results indicate that P. longaeva needles have a maximum photosynthesis rate (Amax) of ~5 µmol CO₂ m^-2 s^-1 at 2-5 years of age followed by a linear decline over the remaining decades of foliar lifespan. Yet, even the oldest foliage, at 45-49 years of age, is still capable of maintaining a positive net CO₂ assimilation rate. We found that the linear decline in Amax over the latter decades of needle lifespan was paralleled by declines in chlorophyll fluorescence and O₂-production based measures of photosynthetic activity as well as foliar concentrations of N_L and chl. It appears that various components of the photosynthetic apparatus are coordinately dismantled in senescing needles. Despite the different time-scales, this pattern of gradual and coordinated photosynthetic decline in P. longaeva is qualitatively similar to that of other species. Other aspects of foliar development in P. longaeva needles were distinct from what is observed in species with much shorter lived leaves. In particular, Amax did not scale with N_L or chl during the first decade of needle development. Rather, foliar N_L and chl gradually increased before peaking in ten-year old needles, while Amax had typically begun declining five years earlier. Photosynthetic senescence in fully mature bristlecone pine needles is qualitatively indistinguishable from foliar senescence in other vascular plant species, but photosynthetic maturation appears to be exceptionally slow and less obviously coordinated in this long-lived foliage.