Qiujie Liu, Mary Galli, Xue Liu, Silvia Federici, Amy Buck, Jon Cody, Massimo Labra, and Andrea Gallavotti

PNAS September 24, 2019 116 (39) 19736-19742

Significance

Meristems are highly regulated groups of stem cells that are ultimately responsible for the formation of all branches, lateral organs, and stems in plants, and thus directly affect plant architecture and crop yield. We have identified a highly conserved member of a family of mitochondria-localized proteases that regulates maize inflorescence architecture. Unlike in Arabidopsis, in which its function appears dispensable, we have discovered that this protein is required for maize growth and productivity in field conditions and in high temperatures, and we provide evidence that it maintains reproductive meristem redox status and auxin homeostasis. These data highlight the importance of meristem redox status for sustaining maize organogenesis in challenging environments.

Abstract

Meristems are highly regulated structures ultimately responsible for the formation of branches, lateral organs, and stems, and thus directly affect plant architecture and crop yield. In meristems, genetic networks, hormones, and signaling molecules are tightly integrated to establish robust systems that can adapt growth to continuous inputs from the environment. Here we characterized needle1 (ndl1), a temperature-sensitive maize mutant that displays severe reproductive defects and strong genetic interactions with known mutants affected in the regulation of the plant hormone auxin. NDL1 encodes a mitochondria-localized ATP-dependent metalloprotease belonging to the FILAMENTATION TEMPERATURE-SENSITIVE H (FTSH) family. Together with the hyperaccumulation of reactive oxygen species (ROS), ndl1 inflorescences show up-regulation of a plethora of stress-response genes. We provide evidence that these conditions alter endogenous auxin levels and disrupt primordia initiation in meristems. These findings connect meristem redox status and auxin in the control of maize growth.

See https://www.pnas.org/content/116/39/19736

Figure 1: ndl1 is defective in reproductive organogenesis. (A–D) The ndl1 tassel phenotype is very variable, from mild (B) to severe (D). (E–H) SEMs of immature tassels in normal and mutant plants also show different expressivity of the ndl1 mutation. AMs, axillary meristems; IM, inflorescence meristem. (Scale bars, 500 μm.) (I–N) mRNA in situ hybridizations of immature tassels with ZYB15, ARF4, and BA1 antisense probes. (Scale bars, 250 μm.) (O and P) Confocal images of normal and ndl1 immature tassels expressing ZmPIN1a-YFP; arrowhead points to PIN1-YFP up-regulation at the site of primordia initiation. (Scale bars, 100 μm.).