Conserved DNA-damage responses (DDRs) efficiently cope with replication blocks and double-strand breaks (DSBs) in cultured eukaryotic cells; DDRs in tissues remain poorly understood. DDR-inactivating mutations lethal in animals are tolerated in Arabidopsis, whose root meristem provides a powerful stem-cell-niche model. We imaged UVB-induced death of specific meristem cells in single and double Arabidopsis mutants to elucidate cooperation among DNA translesion synthesis (TLS) polymerases (Polη, Polζ) and DNA-damage-activated protein kinases (ATR, ATM). Death was 100-fold higher in stem and progenitor (StPr) cells than in transiently amplifying cells. Quantitative analyses of dose–response plots showed that Polη and Polζ act redundantly to tolerate replication blocks and that Polζ-mediated TLS requires ATR. Deficient TLS resulted in ATM-signaled death, which first appeared 10–14h post-UVB. Although ssDNA downstream of blocks was likely cleaved into DSBs throughout S phase, death pathways appeared to initiate late in S. In atm mutants death appeared much later, likely signaled by a slow ATR-dependent pathway. To bypass replication blocks, tissues may use TLS rather than error-free pathways that could generate genomic aberrations. Dynamic balances among ATR and ATM death-avoidance and death-signaling functions determine how many DSB-burdened StPr cells are killed. Their replacement by less-burdened quiescent-center cells then restores growth homeostasis.