NEEDLE1 encodes a mitochondria localized ATP-dependent metalloprotease required for thermotolerant maize growth

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.

Recent Advances in Understanding the Structural and Functional Evolution of FtsH Proteases

“…For example, Arabidopsis mutants lacking FtsH11 fail to grow at 30°C ( Janska et al, 2010 ). A similar phenomenon is observed in the maize ndl-1 mutants ( Liu et al, 2019 ). A striking discrepancy is that a phylogenetic analysis suggests Ndl-1 is an m -AAA protease closely related to FtsH3 and FtsH10 in Arabidopsis .…”

How is auxin linked with cellular energy pathways to promote growth?

“…First, mitochondrial proteases have been shown to be necessary for auxin homeostasis. In maize, mutation of NEEDLE1 ( NDL1 ), a mitochondria‐localized adenosine triphosphate (ATP)‐dependent metalloprotease belonging to the FILAMENTATION TEMPERATURESENSITIVE H ( FTSH ) family, disrupted auxin signalling and transport and lowered the level of free IAA compared to WT (Liu et al ., 2019). Similarly, in Arabidopsis, mutation of FTSH4 correlated with a decrease in IAA concentration and downregulation of several auxin signalling genes (Zhang et al ., 2014).…”

“…Hence, it seems likely that IAA has important roles in controlling the synthesis and degradation rates of key mitochondrial and chloroplast components. Links between proteases of mitochondrial machinery and auxin might be explained by these phenomena (Zhang et al ., 2014; Liu et al ., 2019). Analysis of changes in translation rates in response to auxin, through riboseq (Aspden et al ., 2014; Erhard et al ., 2018) and/or direct measures of protein synthesis (Tivendale et al ., 2021b), would enable this hypothesis to be tested.…”

Outstanding questions in flower metabolism

“…In maize, for example, when high levels of reactive oxygen species (ROS) develop during floral induction, mitochondria switch to the alternative oxidase pathway. This phenomenon, if prolonged in time, may lead to altered inflorescence architecture as in the case of needle 1 mutant (Liu et al ., 2019). The role of AOX during flower anthesis is also not fully known, although a spike in AOX1 and AOX2 gene expression has been observed in tobacco petals and sepals as flowers open (Müller et al ., 2010).…”