Department of Biomolecular Sciences, University of Urbino Carlo Bo, 61029 Urbino, Italy.
National Institute for Nuclear Physics (INFN)-Gran Sasso National Laboratory (LNGS), 67100 Assergi, L'Aquila, Italy.
Cells. 2020 Oct 27;9(11):2362. doi: 10.3390/cells9112362.
This article challenges the notion of the randomness of mutations in eukaryotic cells by unveiling stress-induced human non-random genome editing mechanisms. To account for the existence of such mechanisms, I have developed molecular concepts of the cell environment and cell environmental stressors and, making use of a large quantity of published data, hypothesised the origin of some crucial biological leaps along the evolutionary path of life on Earth under the pressure of natural selection, in particular, (1) virus-cell mating as a primordial form of sexual recombination and symbiosis; (2) Lamarckian CRISPR-Cas systems; (3) eukaryotic gene development; (4) antiviral activity of retrotransposon-guided mutagenic enzymes; and finally, (5) the exaptation of antiviral mutagenic mechanisms to stress-induced genome editing mechanisms directed at "hyper-transcribed" endogenous genes. Genes transcribed at their maximum rate (hyper-transcribed), yet still unable to meet new chronic environmental demands generated by "pollution", are inadequate and generate more and more intronic retrotransposon transcripts. In this scenario, RNA-guided mutagenic enzymes (e.g., Apolipoprotein B mRNA editing catalytic polypeptide-like enzymes, APOBECs), which have been shown to bind to retrotransposon RNA-repetitive sequences, would be surgically targeted by intronic retrotransposons on opened chromatin regions of the same "hyper-transcribed" genes. RNA-guided mutagenic enzymes may therefore "Lamarkianly" generate single nucleotide polymorphisms (SNP) and gene copy number variations (CNV), as well as transposon transposition and chromosomal translocations in the restricted areas of hyper-functional and inadequate genes, leaving intact the rest of the genome. CNV and SNP of hyper-transcribed genes may allow cells to surgically explore a new fitness scenario, which increases their adaptability to stressful environmental conditions. Like the mechanisms of immunoglobulin somatic hypermutation, non-random genome editing mechanisms may generate several cell mutants, and those codifying for the most environmentally adequate proteins would have a survival advantage and would therefore be Darwinianly selected. Non-random genome editing mechanisms represent tools of evolvability leading to organismal adaptation including transgenerational non-Mendelian gene transmission or to death of environmentally inadequate genomes. They are a link between environmental changes and biological novelty and plasticity, finally providing a molecular basis to reconcile gene-centred and "ecological" views of evolution.
本文通过揭示应激诱导的人类非随机基因组编辑机制,挑战了真核细胞中突变随机性的观点。为了解释这些机制的存在,我提出了细胞环境和细胞环境胁迫的分子概念,并利用大量已发表的数据,假设有一些关键的生物学飞跃是在地球生命的进化过程中由于自然选择的压力而产生的,特别是:(1)病毒-细胞交配作为原始形式的性重组和共生;(2)拉马克式的 CRISPR-Cas 系统;(3)真核基因的发展;(4)逆转录转座子引导的诱变酶的抗病毒活性;最后,(5)抗病毒诱变机制的适应进化为应激诱导的针对“高转录”内源性基因的基因组编辑机制。那些以最大速率转录的基因(高转录),仍然无法满足“污染”产生的新的慢性环境需求,是不足的,并产生越来越多的内含子逆转录转座子转录本。在这种情况下,已经证明能够结合逆转录转座子 RNA 重复序列的 RNA 指导的诱变酶(例如载脂蛋白 B mRNA 编辑催化多肽样酶,APOBECs),将被同一“高转录”基因的开放染色质区域上的内含子逆转录转座子靶向。因此,RNA 指导的诱变酶可能会“拉马克式”地在高功能和不足的基因的受限区域中产生单核苷酸多态性(SNP)和基因拷贝数变异(CNV),以及转座子转位和染色体易位,而基因组的其余部分保持完整。高转录基因的 CNV 和 SNP 可能使细胞能够探索新的适应性情景,从而提高其对应激环境条件的适应性。与免疫球蛋白体细胞超突变的机制类似,非随机基因组编辑机制可能产生多个细胞突变体,而那些编码最适应环境的蛋白质的突变体将具有生存优势,因此将被达尔文式选择。非随机基因组编辑机制是可进化性的工具,导致生物适应性,包括跨代非孟德尔基因传递或环境不足基因组的死亡。它们是环境变化和生物新颖性和可塑性之间的联系,最终为协调以基因为中心和“生态”的进化观点提供了分子基础。