Does Shoot Apical Meristem Function as the Germline in Safeguarding Against Excess of Mutations?

Abstract

A genetic continuity of living organisms relies on the germline which is a specialized cell lineage producing gametes. Essential in the germline functioning is the protection of genetic information that is subjected to spontaneous mutations. Due to indeterminate growth, late specification of the germline, and unique longevity, plants are expected to accumulate somatic mutations during their lifetime that leads to decrease in individual and population fitness. However, protective mechanisms, similar to those in animals, exist in plant shoot apical meristem (SAM) allowing plants to reduce the accumulation and transmission of mutations. This review describes cellular- and tissue-level mechanisms related to spatio-temporal distribution of cell divisions, organization of stem cell lineages, and cell fate specification to argue that the SAM functions analogous to animal germline.

Somatic mutation detection: a critical evaluation through simulations and reanalyses in oaks

“…Our reanalysis shows robust evidence for an up to 7-fold higher number of mutations than previously reported, a value closer to the expectations based on the theory (Schoen & Schultz, 2019;Burian, 2021). We argue that knowledge and methodological transfers from cancer to plant mutation detection are expected to contribute strongly to the upward trend of this field and to reconcile empirical reports with theoretical expectations.…”

“…We found that cancer variant callers performed better than generic variant callers for mutation detection at low or intermediate allelic frequency or with low sequencing depth, and similarly well for high allelic frequency. Low allelic frequency mutations, potentially due to the chimeric nature of plant shoot apical meristems structures (Burian, 2021), might be very important due to their great abundance that may balance out their low chance of transmissions. Therefore, plant mutation studies should make greater use of cancer variant callers such as Strelka2 rather than generic variant callers such as GATK to detect somatic mutations, in agreement with previous studies on germline mutations detection (Chen et al ., 2019), especially for detecting low frequency mutations and when using low sequencing depth.…”

Population-level consequences of inheritable somatic mutations and the evolution of mutation rates in plants

“…For instance, investing in a higher fidelity of DNA replication may tend to slow down individual growth. The number of mitoses separating two meristems also depends on patterns of meristematic stem cell divisions that were recently brought to light [39]. Indeed, although it has long been thought that the germline remains unsegregated up until a meristem switches to the floral state in plants, Burian et al [1] showed that within the apical meristem, the stem cells give rise to a specific cell lineage which will serve as the axillary meristems' stem cells and spend most of their time in a quiescent, almost non-dividing state, contrary to surrounding cell lineages which divide vigorously to effect plant growth.…”

“…Thanks to this mechanism, the number of mitoses separating two meristems is greatly reduced and so is the number of cell divisions separating the seed from the gametes, as the germline directly emerges from these stem cells. Hence, although it is clear that the plant germline remains undifferentiated up until reproduction is triggered, it may be considered segregated prior to differentiation, because the cells giving rise to it do not suffer the same fate as surrounding somatic cell lineages, thus behaving as a functional germline [39,40]. The exact timing of such segregation during plant development is, however, not known [3].…”

“…Therefore, it is important to point out that the results presented in this study not only hold if the germline segregates late in development, but that they would also hold if the germline was actually segregated as early as the first embryonic cell division (as it is the case in animals) and remained sheltered within meristems. Indeed, such segregated germline would still have to go through a non-zero number of mitotic cell divisions to be passed from one meristem to the next due to developmental constraints [39], so that the number of cell divisions it goes through before reproduction would still be affected by individual growth and be higher in more long-lived, larger species. In summary, the validity of the results presented in this paper does not depend on the degree to which the germline is actually segregated in plants, but the existence of a functional germline as described above, irrespective of when germline segregation occurs, supports the idea that plants acquired physiological mechanisms favouring lower values of γ.…”