TY - JOUR
T1 - Evolutionary systems biology reveals patterns of rice adaptation to drought-prone agro-ecosystems
AU - Groen, Simon C.
AU - Joly-Lopez, Zo
AU - Platts, Adrian E.
AU - Natividad, Mignon
AU - Fresquez, Zoë
AU - Mauck, William M.
AU - Quintana, Marinell R.
AU - Cabral, Carlo Leo U.
AU - Torres, Rolando O.
AU - Satija, Rahul
AU - Purugganan, Michael D.
AU - Henry, Amelia
N1 - Publisher Copyright:
© 2021 American Society of Plant Biologists. All rights reserved.
PY - 2022/2
Y1 - 2022/2
N2 - Rice (Oryza sativa) was domesticated around 10,000 years ago and has developed into a staple for half of humanity. The crop evolved and is currently grown in stably wet and intermittently dry agro-ecosystems, but patterns of adaptation to differences in water availability remain poorly understood. While previous field studies have evaluated plant developmental adaptations to water deficit, adaptive variation in functional and hydraulic components, particularly in relation to gene expression, has received less attention. Here, we take an evolutionary systems biology approach to characterize adaptive drought resistance traits across roots and shoots. We find that rice harbors heritable variation in molecular, physiological, and morphological traits that is linked to higher fitness under drought. We identify modules of co-expressed genes that are associated with adaptive drought avoidance and tolerance mechanisms. These expression modules showed evidence of polygenic adaptation in rice subgroups harboring accessions that evolved in drought-prone agro-ecosystems. Fitness-linked expression patterns allowed us to identify the drought-Adaptive nature of optimizing photosynthesis and interactions with arbuscular mycorrhizal fungi. Taken together, our study provides an unprecedented, integrative view of rice adaptation to water-limited field conditions.
AB - Rice (Oryza sativa) was domesticated around 10,000 years ago and has developed into a staple for half of humanity. The crop evolved and is currently grown in stably wet and intermittently dry agro-ecosystems, but patterns of adaptation to differences in water availability remain poorly understood. While previous field studies have evaluated plant developmental adaptations to water deficit, adaptive variation in functional and hydraulic components, particularly in relation to gene expression, has received less attention. Here, we take an evolutionary systems biology approach to characterize adaptive drought resistance traits across roots and shoots. We find that rice harbors heritable variation in molecular, physiological, and morphological traits that is linked to higher fitness under drought. We identify modules of co-expressed genes that are associated with adaptive drought avoidance and tolerance mechanisms. These expression modules showed evidence of polygenic adaptation in rice subgroups harboring accessions that evolved in drought-prone agro-ecosystems. Fitness-linked expression patterns allowed us to identify the drought-Adaptive nature of optimizing photosynthesis and interactions with arbuscular mycorrhizal fungi. Taken together, our study provides an unprecedented, integrative view of rice adaptation to water-limited field conditions.
KW - Adaptation, Physiological/physiology
KW - Crops, Agricultural/physiology
KW - Domestication
KW - Droughts
KW - Gene Expression Regulation, Plant
KW - Gene Regulatory Networks
KW - Genetic Variation
KW - Mycorrhizae/physiology
KW - Oryza/physiology
KW - Photosynthesis/physiology
KW - Plant Proteins/genetics
KW - Plant Roots/physiology
KW - Plant Shoots/physiology
KW - Selection, Genetic
KW - Systems Biology
UR - http://www.scopus.com/inward/record.url?scp=85124432967&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85124432967&partnerID=8YFLogxK
U2 - 10.1093/plcell/koab275
DO - 10.1093/plcell/koab275
M3 - Article
C2 - 34791424
AN - SCOPUS:85124432967
SN - 1040-4651
VL - 34
SP - 759
EP - 783
JO - Plant Cell
JF - Plant Cell
IS - 2
ER -