1 Introduction
NASA GISS showed that the average global temperature has increased by about 0.8 ℃ since 1880 (Carlowicz, 2010), and two-thirds of the warming has occurred since 1975 at a rate of about 0.20 ℃ per decade (Masson-Delmotte et al., 2018). The increased temperature and extreme heat stress are continuously restricting agricultural production and threating global food and feed security (Shiferaw, Prasanna, Hellin, & Bänziger, 2011; Rojas-Downing, Nejadhashemi, Harrigan, & Woznicki, 2017; Khaliq, Iqbal, & Zafar, 2019;). As one of most important stable crops, maize (Zea mays L.) is planted over a wider range of altitudes and latitudes than other food crops and under different temperatures ranging from cool to hot. In each region, heat stress may occur at different stages during maize growth, and the occurrences of extreme heat frequently overlap with reproductive growth stage (Hedhly, Hormaza, & Herrero, 2009), hence reducing yield tremendously (Ferris, Ellis, Wheeler, & Hadley, 1998; Wang et al., 2019)
Heat stress can impact maize yield formation at different growth stages, out of which flowering is considered the most susceptible stage (Cicchino, Rattalino Edreira, & Otegui, 2010; Siebers et al., 2017). Temperature beyond 30.5 ℃ advances tasseling and pollen shedding (Schoper, Lambert, Vasilas, & Westgate, 1987; Sanchez, Rasmussen, & Porter, 2014) but has smaller effects on silking dynamics, hence extending anthesis – silking interval (ASI) (Rattalino Edreira, Budakli Carpici, Sammarro, & Otegui, 2011; Lizaso et al., 2018; Wang et al., 2019). Pollen shedding number dramatically reduces in > 36 ℃ condition due to the failed anther dehiscence (Wang et al., 2019), and pollen viability is greatly reduced by temperature > 38 ℃ because of the disturbed pollen structure and components in maize (Herrero & Johnson, 1980; Muchow & Carberry, 1989; Sanchez et al., 2014). In the study of Cicchino, Rattalino Edreira, Uribelarrea, & Otegui (2010), nonheated fresh pollens were supplied to heated silked ears and remained at heat condition for 15 days, and kernel number reduced by more than 60%. A cross pollination test (i.e., normal fresh pollens and normal silks were crossed pollinated and were transferred to heat stress) showed that pollination and fertilization processes were also sensitive to high temperature in maize (Wang et al., 2019). Post-silking heat stress even in a short episode likely resulted in kernel abortion and reduced kernel number which implied that early seed development was sensitive to heat stress in maize (Sehgal et al., 2018). Pollen tube growth, fertilization, and the subsequent growth and development of the embryo and endosperm can be disrupted by post-pollination high temperature in rice (Oryza sativa L., Shi et al., 2017), sorghum (Sorghum bicolor L., Chiluwal et al., 2020), and wheat (Triticum aestivum L., Jagadish, 2020). The relevant evidences, however, are still limited in maize, and the mechanisms remain to be tested (Smith, 2019).
Compared to kernel number, the extent to which high temperature reduces kernel weight was much smaller during flowering in maize (Wilhelm, Mullen, Keeling, & Singletary, 1999; Suwa et al., 2010; Wang et al., 2019). Kernel weight in 14-day high temperature 40/30 ℃ (day/night) that bracket the silking stage was at the same level with in 32/22 ℃ (Wang et al., 2019). However, a 6-day continuous 35 ℃ temperature that begun 5 d after pollination reduced kernel weight by 95% for maize inbred lines B73 (Commuri & Jones, 2001), suggesting early grain filling period is sensitive to high temperature. Many studies indicated that heat stress at early grain filling increases the protein content and reduces the starch content in grains (Thitisaksakul, Jiménez, Arias, & Beckles, 2012; Mayer, Savin, & Maddonni, 2016; Yang, Gu, Ding, Lu, & Lu, 2018). In the study of Ben-Asher, Garcia, & Hoogenboom (2008), the net photosynthetic rate (Pn) in maize was reduced by 50 – 60% in high temperature of 35/30 – 40/35 ℃ compared to 25/20 – 30/25 ℃. The insufficient photosynthates accumulation for grain filling resulted from the decreased enzyme activities and relative transcript levels of genes (Duke & Doehlert, 1996). Additionally, heat stress at early grain filling in wheat accelerated grain filling rate but shortened the duration; the former did not compensate for loss of the latter, thereby resulting in a small grain size and low kernel weight (Farooq, Bramley, Palta, & Siddique, 2011). The relevant studies of heat stress occurring after pollination in maize, however, are limited, and are still unable to fully reveal the mechanism of its influence on kernel weight.
It has been confirmed that maize hybrids with different genetic backgrounds responded differently to heat stress around flowering (Suwa et al., 2010; Rattalino Edreira et al., 2011; Rattalino Edreira & Otegui, 2012, 2013; Rattalino Edreira, Mayer, & Otegui, 2014). Tropical maize hybrids conferred a higher capacity for enduring heat effects than temperate maize when forming kernels by synchronizing anthesis and silking time (Rattalino Edreira et al., 2011). Evidences also indicated that tropical maize lines showed a broader adaption to multi-environmental conditions especially for the lines that derived from lowland sites (Jiang et al., 1999; Abadassi & Herve, 2000). Although tropical maize contains many ecotypes with interesting adaptation traits, this germplasm has some undesirable traits such as late maturity, excessive plant or ear height, and low harvest index (Abadassi & Herve, 2000; White, Vincent, Moose, & Below, 2012; Edmeades, Trevisan, Prasanna, & Campos, 2017). Hence, tropical germplasm was incorporated into temperate lines to achieve high yield potential, adaptability and stability of maize (Lafitte & Edmeades, 1997; Lewis & Goodman, 2003; Wolde, Keno, Tadesse, Bogale, & Abebe, 2018). Mushayi, Shimelis, Derera, Shayanowako, & Mathew (2020) compared 117 maize hybrids at five location in South Africa and found that hybrids derived from temperate × tropical inbred lines exhibited a higher yield and broader adaption compared to the hybrids developed from either temperate or tropical germplasms. These results clearly reveal the important implication of germplasm when selecting of and breeding for superior hybrids for broad and specific adaptation to the target environments. However, responses of different maize germplasms (i.e., temperate, tropical, and temperate × tropical) to high temperature or extreme heat events have not widely evaluated and compared so far in terms of flowering dynamics and kernel formation.
Therefore, 162 maize inbred lines including 40 temperate lines, 45 tropical lines, and 77 temperate × tropical inbred lines were sown at different sowing dates in four experimental years (i) to evaluate their responses to heat stress around flowering and during the early grain filling period; and (ii) to explain the underlying mechanisms from the perspective of flowering characteristic.