Table 1.
Genetic mapping and candidate genes for nine physiological responses to chilling stress in maize
| Study | Genetic variation | Genetic mapping | Candidate genes |
|---|---|---|---|
| CO 2 assimilation rate | |||
| F2:3 population from chilling-tolerant (ETH-DH7) and chilling-sensitive (ETH-DL3) lines. 15/13 °C for whole life following establishment; measured leaf 3 (Fracheboud et al., 2004) | Yes | Yes—QTL for carbon exchange rate (a measurement of CO2 assimilation)a | No |
| 233 RILs from drought-tolerant (Ac7643) and drought-susceptible (Ac7729/TZSRW) lines. 15/13 °C for whole life following establishment; measured leaf 3 (Fracheboud et al., 2002) | Yes | Yes—QTL for CO2 fixation; eight regions with QTL for photosynthetic traits; pericentromeric region of chromosome 3 a key locationb | No |
| 226 F2:3 families from ETH-DH7×ETH-DL3 and 168 F2:4 from Lo964×Lo1016 (different chilling tolerance at germination and different root morphology). 15/13 °C for 14 d following establishment; measured leaf 3 (Hund et al., 2005) | Yes | Yes—QTL for carbon exchange rate | No |
| 282 inbred lines. 8 °C at germination (Hu et al., 2017) | Carbon exchange rate not measured directly | Yes—SNPs related to carbon exchange rate in other studies | Yes—identified 18 candidate genes in totalc |
| 49 inbred lines. 15/13 °C at 7 leaf stage, measured leaf 8 (Lee et al., 2002) | Yes | No | No |
| PSII operating efficiency (ΦPSII) | |||
| F2:3 population from ETH-DH7×ETH-DL3. Early and late sowing in the field provided chilling treatment (Jompuk et al., 2005) | Yes | Yes—QTL for ΦPSII located on chromosomes 2, 4, 6, 8, 9 (most prominent on 6) | No |
| Population from chilling sensitive×tolerant inbred lines. 14/8 °C for the duration of the experiment. (Rodríguez et al., 2014) | Yes | Yes—two QTL for maintenance of ΦPSII in chilling stressd | No |
| Fracheboud et al. (2004) | Yes | Yes—QTL for ΦPSII | No |
| Fracheboud et al. (2002) | Yes | Yes—QTL for ΦPSII | No |
| Hund et al. (2005) | Yes | Yes—QTL for ΦPSII, located on different chromosomes in the different populations | No |
| 168 F2:4 families from Lo964×Lo1016 (see above). 15/13 °C for the duration of the experiment; measured at first leaf stage (Hund et al., 2004) | Yes | Yes—four QTL for ΦPSII | A locus for ΦPSII was identified |
| One chilling-tolerant and one chilling-sensitive line. (ETH-DH7 and ETH-DL3). 8/6 °C imposed for 14 h at third leaf stage (Sobkowiak et al., 2014) | Yes | Yes—DEGs adjacent to QTL for chlorophyll fluorescence | Yes—overall, identified 66 genes responding differently between lines (DEGs) |
| Lee et al. (2002) | Yes | No | No |
| Two panels: 306 Dent lines and 292 Flint lines. 14/8 °C for duration of experiment (Revilla et al., 2016) | Yes | Yes—two SNPs for ΦPSII in chilling stress in Flint population (chromosomes 1, 4); QTL for ΦPSII. Overall, more QTL for chilling tolerance were identified in the Flint panel |
Yes—performed GWAS and identified candidate genes |
| Three breeding groups, total 375 inbred lines. 16/13 °C. (Strigens et al., 2013) | Yes—significant differences in ϕPSII between the breeding groups | Yes—identified three QTL for ΦPSII (two under chilling stress, one only under optimal conditions) | No |
| Photosynthetic gene expression | |||
| Sobkowiak et al. (2014) | Yes | Yes—DEGs adjacent to QTL for C4 enzymes | Yes (see above) |
| One chilling-tolerant (S68911) and two chilling-sensitive lines (S160 and S50676). 14/12 °C for 4 d then 8/6 °C for 4 d at third leaf stage (Sobkowiak et al., 2016) | Yes | No | Yes—GO enrichment identified photosynthetic genes |
| Two unrelated inbred lines: CG60, CG102. 14/2 °C for 3 d at second leaf stage; measured after 1 d chilling (Avila et al., 2018) | Yes | No | Yes—GO term analysis identified photosynthetic genes down-regulated in chilling stress |
| Four stress-sensitive ‘Lancaster’ lines, four tolerant lines. 6/4 °C for 24 h at fourth leaf stage (Banović Đeri et al., 2021) | Yes | No | Yes—seven DEGs including photosynthetic genes. Differential expression between genotypes and treatment/control and between genotypes |
| One chilling-tolerant (M54), one chilling-sensitive (753F) line. 4 °C chilling stress for up to 24 h at fourth leaf stage (Li et al., 2019) | Yes | No | Yes—chilling stress affected photosynthetic genes |
| One chilling-tolerant (B144), one-chilling sensitive (Q319) line. 5 °C chilling stress for 12 h or 24 h at third leaf stage (Yu et al., 2021) | Yes | No | Yes—up-regulation of the D1 protein psb29 after 24 h (following initial decrease at 12 h) enabled B144 to protect PSII from photooxidation |
| Non-photochemical quenching (NPQ) | |||
| Fracheboud et al. (2002) | Yes | Yes—QTL for xanthophylls | No |
| A chilling-sensitive inbred line (A661) and B73. 15 °C for the duration of the experiment (Rodríguez et al., 2013) | Yes—lower xanthophylls in A661 | No | No |
| Chlorophyll content | |||
| 302 RILs from B73×Mo17. 14/8 °C for the experiment duration; measured after 30 d (Rodríguez et al., 2008) | Yes—measured chlorophyll using optical scale | Yes—QTL identified on chromosomes 3 and 6, under chilling conditions onlye | QTL on chromosome 6 may correspond to luteus11 locus |
| Fracheboud et al. (2004) | Yes | QTL identified on chromosome 3 | No |
| Fracheboud et al. (2002) | Yes | Yes—QTL for chlorophyll | No |
| Hund et al. (2005) | Yes | Yes—QTL for chlorophyll | No |
| Hu et al. (2017) | Chlorophyll not measured directly | Yes—SNPs related to chlorophyll in other studies | Yes—see above |
| Two populations of field×sweet corn (B73×P39, 179 RILs; B73×IL14 h, 213 RILs). 14/10 °C for the experiment duration (Allam et al., 2016) | Yes | Yes—QTL for chlorophyll content | No |
| Hund et al. (2004) | Yes | Yes—seven QTL for chlorophyll | No |
| 76 accessions. 10/8 °C for whole life, measured at fourth leaf stage (Bano et al., 2015) | Yes | No | No |
| Sobkowiak et al. (2014) | Chlorophyll not measured directly | Yes—DEGs adjacent to QTL for chlorophyll content | Yes—see above |
| Lee et al. (2002) | Yes | No | No |
| Jompuk et al. (2005) | Yes | Yes—six QTL on chromosomes 1, 2, 3, 4, 10 in early-sown plants; four QTL in late-sown plantsf | No |
| Avila et al. (2018) | Yes | No | Differential expression of chloroplast genes under chilling stress |
| Rodríguez et al. (2013) | Yes—lower chlorophyll and higher chlorophyllase activity in A661 | Yes—QTL on chromosome 2 for chilling-induced albinismg | Yes—a putative gene in chlorophyll biosynthesis, and a chlorophyll-binding protein |
| Revilla et al. (2016) | Yes | Yes—two SNPs for chlorophyll in chilling stress in Dent population (chromosomes 1, 4) | Yes |
| Antioxidant enzymes, or oxidative damage | |||
| Association panel of 125 inbred lines. 6.4 °C for 7 d at third leaf stage (Huang et al., 2013) | Not measured directly | No | Candidate genes in five categories including one for antifreeze and H2O2 removal |
| Sobkowiak et al. (2014) | Not measured directly | Yes—DEGs adjacent to QTL related to antioxidant levels | Genes for antioxidant systems identified |
| Tolerant (S68911) and sensitive (B73) inbred lines. 14/10 °C for the duration of the experiment, measured at early growth stages (Jończyket al., 2021) | Not measured directly, but transcriptomic data suggest greater ROS scavenging in S68911 in chilling conditions | No | No; examined stress-response motifs and chromatin accessibility, related to chilling tolerance in the tolerant line which switched from growth to defence |
| Abscisic acid (ABA) | |||
| Jończyk et al. (2021) | Not measured directly, but transcriptomic data suggest greater ABA synthesis in tolerant line in chilling conditions | No | No—but see above |
| Leaf sugar content | |||
| Tolerant (S68911) and sensitive (S160) inbred lines. 14/12 °C for 28 h at third leaf stage (Bilska-Kos et al., 2016) | Yes—decreased phloem loading in sensitive line was observed; this leads to increased leaf sugars (not measured) | No | Yes—expression of genes involved in phloem loading |
| Leaf expansion | |||
| Huang et al. (2013) | Yes | Yes—SNPs for shoot length identified | Yes—13 genes involved in biosynthesis, metabolism, cell division, and growth |
Synthesis of studies including more than one genotype and measuring physiological responses to chilling stress. Studies are grouped according to the order of responses presented in Fig. 2. When describing each study, only chilling temperatures are included; control temperatures are omitted for brevity. Studies are listed under each applicable category but only described at the first instance.
a QTL for a range of traits explained between 37% and 54% of the phenotypic variance in this study.
b QTL explained up to 20% of phenotypic variance in this study.
c Of these 18 genes, 10 were supported by other studies and three were novel.
d These two QTL explained 19% and 6% of phenotypic variance.
e The QTL on chromosome 6, probably at the end of bin 6.03, is located near to—and may be the same as—the QTL at bin 6.04 in the IBM2 2005 Neighbors 6 map, identified by Fracheboud et al. (2004). These may correspond to the luteus11 locus which affects leaf colour (Rodríguez et al., 2008).
f A QTL related to leaf greenness on chromosome 3 was identified as being the same as a previously identified QTL related to photosynthesis, in a population derived from the same parent lines (Fracheboud et al., 2004). Of the four QTL in late-sown plants, three were common with the early-sown plants.
g This QTL explains 14% of phenotypic variation in chilling-induced albinism.